During neural recordings, monkeys viewed a display consisting of two square planar objects that were defined by random dot patterns (Figure 1A, B; Figure 1—figure supplement 1; Video 1; see Methods for details). The animal viewed these objects while being translated (0.5 Hz modified sinusoid, see Methods) along an axis in the fronto-parallel plane which corresponded with the preferred-null motion axis of the neuron under study. In the base condition of the task with no cue conflict between depth from disparity and motion parallax, both objects were simulated to be stationary in the world, such that their image motion was determined by the self-motion trajectory and the location of the objects in depth. When the objects were stationary in the world, their depth defined by motion parallax and disparity cues was the same, hence the difference in depth between the two cues was zero (ΔDepth = d_MP – d_BD = 0).

Figure 1 with 3 supplements see all

Download asset Open asset

Video 1

Download asset

In other conditions (ΔDepth ≠ 0), one of the objects was stationary in the world while the second ‘dynamic’ object moved in space such that its depth defined by motion parallax, d_MP, was not consistent with its depth defined by binocular disparity, d_BD (Figure 1B, Figure 1—figure supplement 1B; see Methods for details). As a result of this cue conflict between disparity and motion parallax, the dynamic object should appear to be moving in the world based on previous work in humans (Rushton et al., 2007). As ΔDepth becomes greater in magnitude, it should be easier for the animal to correctly determine which object is the dynamic object. Animals indicated their decision by making a saccade to one of two targets that appeared at the locations of the two objects at the end of the trial (Figure 1A). Critically, due to the experimental design (see Methods for details), animals could not simply detect the dynamic object based on its retinal image velocity since the stationary object(s) in the display also moved on the retina due to self-motion combined with depth variation.

Average psychometric functions for the two animals across 104 recording sessions are shown in Figure 1C. As expected, the animals perform at chance when ΔDepth = 0, and their percent correct increases with the magnitude of ΔDepth. This demonstrates that monkeys can perform the task as expected from human behavioral work (Rushton et al., 2007). Furthermore, we found that performance was near chance levels in a control experiment without binocular disparity cues (Figure 1—figure supplement 2), as also expected from previous work (Rushton et al., 2007).

The ranges of depths of the stationary and dynamic objects were overlapping but not identical (see Methods). To determine whether the animals primarily made their decisions based on ΔDepth and not based upon the individual depths specified by disparity or motion parallax, we performed a logistic regression analysis to determine how animals perceptually weighted depth from motion parallax (|d_MP|), depth from binocular disparity (|d_BD|), and the magnitude of ΔDepth ($\left|d_{MP}-\mathrm{}{d}_{BD}\right|$ ; see Methods for details). Results show that animals primarily weighted the |ΔDepth| cue to make their decisions (Figure 1D, E), although there were small contributions from the individual depth cues. We initially trained each animal to perform the task with four objects present in the display (three stationary objects and one dynamic object), as well as three different pedestal depths, to make it more difficult for animals to rely on d_MP or d_BD. Indeed, we found that the logistic regression weights were also strongly biased in favor of |ΔDepth| in the four-object version of the task (Figure 1—figure supplement 3D, E). To increase the number of stimulus repetitions we could perform during recording experiments, we simplified the task to the two-object case.

We measured the tuning of well-isolated MT neurons for depth defined by either binocular disparity or motion parallax cues, as described previously (Nadler et al., 2013, see also Methods). Receptive fields (RFs) and direction preferences of the population of MT neurons are summarized in Figure 2—figure supplement 1. Figure 2A shows data for a typical ‘congruent’ cell, which prefers near depth defined by both disparity and motion parallax cues (see Methods for definition of congruent and opposite cells). Note that motion parallax stimuli are presented monocularly, such that selectivity for depth from motion parallax cannot be a consequence of binocular cues. In contrast, Figure 2B, C show data for two examples of ‘opposite’ cells that prefer near depths defined by motion parallax and moderate far depths defined by binocular disparity. Such neurons would, in principle, respond more strongly to some stimuli with discrepant disparity and motion parallax cues. Note that, for all of the example cells in Figure 2A–C, responses to binocular disparity are substantially greater than responses to motion parallax. This is mainly because binocular disparity tuning was measured with constant-velocity stimuli at the preferred speed, whereas the range of speeds used to measure depth tuning based on motion parallax is generally lower (and covaries with depth magnitude).

Figure 2 with 1 supplement see all

Download asset Open asset

As done previously (Nadler et al., 2008; Nadler et al., 2009; Nadler et al., 2013; Kim et al., 2015a, Kim et al., 2015b; Kim et al., 2017), we quantified the depth-sign preference of each MT neuron using a depth-sign discrimination index (DSDI, see Methods), which takes on negative values for neurons with near preferences and positive values for neurons with far preferences. Across the population of 123 neurons, depth-sign preferences for motion parallax tended to be strongly biased toward near-preferring neurons, as reported previously (Nadler et al., 2008; Nadler et al., 2013), whereas depth-sign preferences for binocular disparity were rather well balanced (Figure 3A). Importantly, there are roughly equal numbers of neurons in the lower-left and upper-left quadrants of Figure 3A, indicating that congruent and opposite cells were roughly equally prevalent in our sample of MT neurons (see also Nadler et al., 2013). Thus, there are many opposite cells in MT that might respond selectively to dynamic objects over static objects.

Figure 3

Download asset Open asset

Figure 2D shows responses of the example congruent cell (from Figure 2A) that were obtained during the object detection task. Responses to the stationary object (red) are plotted as a function of the depth values specified by motion parallax (which are necessarily equal to binocular disparity values for a stationary object). Responses to the dynamic object (blue) are plotted as a function of both depth defined by motion parallax (lower abscissa) and depth defined by disparity (upper blue abscissa). This allows the reader to determine the depth value for each cue that is associated with a dynamic object having a particular ΔDepth value. For this example congruent cell (Figure 2D), responses to stationary objects with large near depths substantially exceeded responses to any dynamic object.

A strikingly different pattern of results is seen for the example opposite cell in Figure 2E. In this case, there are a few dynamic objects for which the neuron’s response (blue) clearly exceeds the response to stationary objects of all different depth values (red). More specifically, this incongruent cell responds most strongly to dynamic objects that have large near depths defined by motion parallax and depths near the plane of fixation (0 deg) as defined by binocular disparity. This pattern of results is expected from the individual tuning curves in Figure 2B and demonstrates that this opposite cell is preferentially activated by a subset of dynamic objects. The second example opposite cell in Figure 2C, F shows a generally similar pattern of results. For this cell, peak responses to stationary and dynamic objects are similar, but the neuron responds more strongly to dynamic objects over most of the stimulus range. Since we applied our ΔDepth manipulation around a fixed pedestal depth of –0.45 deg (to facilitate decoding, see Methods), we do not expect dynamic objects to preferentially activate every opposite cell. However, cells that are preferentially activated by dynamic objects should tend to be neurons with mismatched depth tuning for motion parallax and binocular disparity cues.

Figure 3B shows that this expected relationship holds across our population of MT neurons. The ratio of peak responses for dynamic:stationary objects is plotted as a function of the correlation coefficient, R_{MP_BD}, between depth tuning curves for disparity and motion parallax. Neurons with R_{MP_BD} < 0 (opposite cells) tend to have peak response ratios that lie in the upper-left quadrant, indicating that opposite cells tend to be preferentially activated by dynamic objects. In contrast, neurons with R_{MP_BD} > 0 (congruent cells) tend to have peak response ratios in the lower-right quadrant, indicating that they tend to be preferentially activated by stationary objects. Across the population, peak response ratio is significantly anti-correlated with R_{MP_BD} (n=106, Spearman rank correlation, R = −0.39, p=2.8×10^–5), indicating that the hypothesized relationship between tuning congruency and response to scene-relative object motion is observed.

We further tested whether differences in depth tuning curves for binocular disparity and motion parallax can predict whether neurons prefer positive or negative ΔDepth values. Using responses to the dynamic object, we quantified each neuron’s preference for positive/negative ΔDepth values using a variant of the DSDI metric, DSDI_dyn (see Methods), and found that it is robustly correlated with the difference in DSDI values (ΔDSDI) computed from depth tuning curves for disparity and motion parallax (Figure 3C, R=0.54, p=2.7×10^–9, n=106, Spearman correlation). Thus, selectivity for ΔDepth during the detection task is reasonably predictable from the congruency of depth tuning measured during a fixation task.

If neurons with mismatched depth tuning for disparity and motion parallax cues are selectively involved in detecting scene-relative object motion, we hypothesized that neurons that respond preferentially to dynamic objects should have responses that are more strongly correlated with perceptual decisions. To measure the correlation of neural activity with perceptual decisions, we took advantage of the fact that our design included a subset of trials in which both objects were stationary in the world and were presented at the pedestal depth of –0.45 deg (Figure 4A). These conditions allowed us to quantify choice-related activity, for a fixed stimulus, by sorting responses into two groups: trials in which the monkey chose the object in the neuron’s RF, and trials in which the monkey chose the object in the opposite hemi-field.

Figure 4 with 1 supplement see all

Download asset Open asset

Data for an example neuron (Figure 4B) show somewhat greater responses when the monkey chose the object located in the neuron’s RF. We quantified this effect by applying ROC analysis to the two choice distributions (see Methods for details), which yielded a detection probability (DP) metric. DP will be greater than 0.5 when responses are greater on trials in which the monkey reported that the stimulus in the RF was the dynamic object. Because DP is only computed from the subset of trials with ΔDepth=0, this measure need not have any relationship with a neuron’s preference for dynamic vs. stationary stimuli. For the example neuron of Figure 4B, the DP value was 0.75, which is significantly greater than chance by permutation test (p=0.006, see Methods). Across a population of 92 neurons for which there were sufficient numbers of choices toward each stimulus (see Methods), the mean DP value of 0.56 was significantly greater than chance (p=6×10^–5, t(91) = 4.21, n=92, t-test) with 13 of 92 neurons showing individually significant DP values (Figure 4C, filled bars). All neurons with significant DP values had effects in the expected direction, with DP>0.5. In addition, the mean DP value was significantly greater than chance for each monkey individually (M1: n=39, mean=0.59, p=5.7×10^–4, t(38) = 3.76; M2: n=53, mean = 0.53, p=0.03, t(52) = 2.21, t-test).

Figure 4 shows that many MT neurons have responses that are correlated with detection choices in the task. We hypothesized that neurons with DP>0.5 are more likely to be those that respond preferentially to dynamic objects over stationary objects. To obtain a signal-to-noise measure of each neuron’s selectivity for dynamic vs. stationary objects, we again applied ROC analysis as illustrated for an opposite cell in Figure 5A–C. This neuron responded more strongly to dynamic objects than stationary objects across most of the depth range (Figure 5A). To quantify this selectivity, for each value of ΔDepth, responses were sorted into two groups: trials in which the dynamic object was in the RF, and trials in which the dynamic object was located in the opposite hemi-field and a stationary object was in the RF (regardless of the depth of the stationary object). Thus, the ROC value computed for each ΔDepth value gave an indication of how well the neuron discriminated between that particular dynamic object and stationary objects of any depth. By convention, ROC values >0.5 indicate greater responses for a dynamic object in the RF.

Figure 5 with 1 supplement see all

Download asset Open asset

Results of this analysis for the example opposite cell (Figure 5B) show that ROC values were greater than 0.5 for all ΔDepth ≠ 0; thus, this neuron reliably responded more strongly to dynamic objects than to stationary objects. To obtain a single metric for each neuron, we simply averaged the ROC metrics for each non-zero ΔDepth value, yielding a neurometric performance (NP) value of 0.78 for this neuron. The corresponding DP value for this neuron was 0.77 (Figure 5C, p=0.0015, permutation test), indicating that this neuron shows both strong selectivity for dynamic objects when ΔDepth ≠ 0 and stronger responses when the animal reports a dynamic object in the RF when ΔDepth = 0.

Data for an example congruent cell (Figure 5D–F) show a very different pattern of results. This neuron generally responds more strongly to stationary objects of any depth than to dynamic objects (Figure 5D). As a result, ROC values are consistently <0.5 when comparing responses to dynamic vs. stationary objects in the RF (ΔDepth ≠ 0, Figure 5E), yielding an NP value of 0.23. The corresponding DP value for this neuron (Figure 5F) was 0.39 (p=0.26, permutation test), indicating that it responded slightly more to ambiguous stimuli when the monkey reports that the object in the RF was stationary. Thus, the data from these two examples neurons support the hypothesis that neurons with preferences for dynamic objects are selectively correlated with perceptual decisions.

To examine whether this hypothesis holds at the population level, we plotted the DP value for each neuron against the corresponding NP value. These two metrics, which are computed from completely different sets of trials (ΔDepth = 0 for DP; ΔDepth ≠ 0 for NP), are strongly correlated (Figure 5G, R=0.47, p=3.2×10^–6, n=92, Spearman rank correlation) such that neurons with DP values substantially greater than 0.5 tend to be neurons that are selective for dynamic objects (NP >0.5). In addition, we observed a significant positive correlation for each animal individually (M1: n=39, R=0.59, p=7.9×10^–5; M2: n=53, R=0.33, p=0.015, Spearman correlation). It is also worth noting that all neurons with large DP values (>0.7) also have NP values substantially greater than 0.5. Thus, the MT neurons that most strongly predict decisions to detect the dynamic object (on ambiguous trials) are those with a consistent preference for dynamic objects.

It is worth noting that the distribution of NP values in Figure 5G is biased toward values >0.5; indeed, the mean NP value (0.56) is significantly greater than 0.5 (one-sample t-test, t(105) = 4.98, and p=2.5×10^–6). This effect likely arises due to the distribution of stimulus values involved in the dynamic object condition. Because neurons were generally tested with a pedestal depth of –0.45 deg, the depth values for both disparity and motion parallax tend to be mostly negative for the dynamic object condition (see blue and black x-axes in Figure 2D–F). This bias toward negative (near) depth values of dynamic objects, combined with the fact that most neurons have a near preference for depth from motion parallax (Figure 3A), means that many neurons (including congruent cells) tend to have mean responses to dynamic objects that are greater than the mean response to stationary objects (e.g. Figure 2D). This asymmetry leads to a mean NP value >0.5.

How is the result of Figure 5G related to neurons’ preference for dynamic relative to stationary objects? Figure 5—figure supplement 1A shows that NP is robustly correlated with peak response ratio (R=0.43, p=4.5×10^–6, Spearman rank correlation). Neurons with peak response ratios substantially greater than unity almost always have NP >0.5. However, some neurons with peak response ratios near unity also have high NP values (including the neuron in Figure 2C, F). In contrast, we did not find a significant correlation between DP and peak response ratio (Figure 5—figure supplement 1B: R=0.12, p=0.25). A main reason for this appears to be that there is a cluster of neurons with large peak response ratios that have DP values near 0.5. These neurons generally have tuning properties similar to the example cell in Figure 2B, E. While incongruent tuning creates a clear preference for dynamic objects for these neurons, that preference is limited to a narrow range of depth values, such that NP values tend to be only modestly >0.5. To achieve high NP values, neurons need to have a consistent preference for dynamic objects (e.g. Figures 2F and 5A). Thus, what seems to be crucial for producing high DP values is that a neuron consistently prefers dynamic objects over the range tested. This explains the robust correlation between DP and NP (Figure 5G) and the weak correlation between DP and peak response ratio (Figure 5—figure supplement 1B). Thus, incongruent tuning tends to lead to a preference for dynamic objects (high peak response ratio, Figure 3B), but does not always lead to high DP values (Figure 5—figure supplement 1B).

We also examined the time course of choice-related activity and found that it appeared within a few hundred ms after the onset of self-motion (Figure 4—figure supplement 1). This choice-related activity was largely sustained throughout the rest of the stimulus period, even when motion of the object was in the anti-preferred direction.

The results described above suggest that perceptual detection of dynamic objects might be driven by the activity of MT neurons with depth tuning curves that make them respond preferentially to dynamic objects. To further probe this hypothesis, we trained a simple linear decoder to detect dynamic objects based on simulated responses of a population of neurons that is closely based on our data, and we examined whether performance of the decoder shows a similar relationship between DP and NP (see Methods for details).

In the simulation (as in the experiments), the dynamic object could appear in either the right or left hemi-field, and the decoder was trained to report the location of the dynamic object. For each neuron in the population, responses were simulated to have the same mean and SD as empirically measured responses. Since neurons were recorded separately and we could not measure correlated noise, we simulated responses based on either independent noise or correlated noise (see Methods for details).

The decoder was trained to report the location of the dynamic object based on simulated population responses from the subset of trials for which ΔDepth ≠ 0. The trained decoder was then used to predict responses for the completely ambiguous (ΔDepth = 0) trials in which identical objects were presented in both hemi-fields. Responses to ambiguous trials were then sorted according to the decoder output to compute predicted DP values (DP_pred) for each neuron in the population.

We first compared DP_pred with NP values for simulations in which all neurons were assumed to have independent noise. This decoder performs very well based on a sample of 97 MT neurons (Figure 6A, see Methods for selection criteria), indicating that there is extensive information available in a moderately sized sample of MT neurons. We find a significant positive correlation between DP_pred and NP (Figure 6B, R=0.53, p=4.9×10^–8, n=97, Spearman correlation) in this simulation, consistent with the empirical observations of Figure 5G. The decoding weights provide an indication of how neurons with different properties contribute to the classification outcomes. With independent noise, we find a strong relationship (Figure 6C, R=0.92, p<1×10^–15, n=97, Spearman correlation) between DP_pred and decoding weights, with positive readout weights being associated with DP_pred values greater than 0.5.

Figure 6

Download asset Open asset

While the relationship between DP_pred and NP in Figure 6B has a positive slope, DP_pred values tend to be substantially closer to 0.5 than the values observed experimentally (Figure 5G). However, this is not surprising given that neurons in this simulation were assumed to have independent noise. It is well established that neurons in MT exhibit correlated noise (e.g. Zohary et al., 1994; Huang and Lisberger, 2009) and that choice-related activity is expected to be stronger in the presence of correlated noise (Britten et al., 1996; Shadlen et al., 1996; Haefner et al., 2013; Gu et al., 2014; Pitkow et al., 2015). Thus, we also simulated responses with a moderate level of correlated noise (median R_noise = 0.15, see Methods for details), which had little impact on decoder performance (Figure 6D). In the presence of correlated noise, DP_pred values show a greater spread around 0.5 and are much more strongly correlated with NP values (Figure 6E, R=0.89, p<3×10^–16, n=92, Spearman correlation). While correlated noise enhances the relationship between DP_pred and NP, it also weakens the relationship between DP_pred and decoding weights (Figure 6F, R=0.46, p=3.4×10^–6, n=92, Spearman correlation), as expected from theoretical studies (Haefner et al., 2013).

These simulations show that our main experimental finding is recapitulated by a simple linear decoder that is trained to distinguish between dynamic and static objects based on MT responses. Note, however, that we have not attempted to find parameters of our decoding simulations that would best match the empirical data (Figure 5G). This would almost certainly be possible, but we do not feel that it is a worthwhile exercise given that we would have to make assumptions about the structure of correlated noise that we cannot sufficiently constrain.

To further assess whether neurons with incongruent tuning for disparity and motion parallax can provide a greater contribution to detecting scene-relative object motion, we performed additional decoding simulations after dividing the population into subgroups based on peak response ratio. Four subgroups were defined: lowest third, middle third, highest third, and a random subsample of the same size from all neurons. Figure 7A shows that decoding performance is significantly greater for the subgroup of neurons with the highest peak response ratios, as compared with the low and middle subgroups (error bars denote 95% CIs). We also performed a similar analysis after dividing the population based on the correlation between depth tuning from disparity and motion parallax cues, R_{MP_BD}. This revealed parallel results in which neurons with the most negative values of R_{MP_BD} achieved significantly greater decoding performance (proportion correct: 0.88±0.008, mean ±95% CIs) than neurons with intermediate (0.82±0.01) or high (0.84±0.009) values of R_{MP_BD}.

Figure 7

Download asset Open asset

We further examined whether detection probabilities predicted by the decoder depend on tuning congruency, using the same subgroups based on peak response ratio. We find that DP_pred values from these decoding simulations are greatest for neurons with the highest peak response ratios, and not significantly above chance for neurons with the lowest peak response ratios (Figure 7B, see caption for details). These results demonstrate that neurons with incongruent tuning carry enhanced information for detecting moving objects during self-motion.

Together, these decoding simulations demonstrate that a population of MT neurons with the depth tuning properties that we have described could be utilized to detect scene-relative object motion, and that such a read-out could produce the relationship between DP and NP that we have observed empirically. The simulations further indicate that neurons with larger peak response ratios provide better decoding performance, consistent with the idea that incongruent tuning is adaptive for detecting object motion during self-motion.

In many instances, scene-relative object motion produces components of image motion that differ clearly in velocity or timing from the background optic flow at the corresponding location. Human observers can detect object motion when there are sufficient differences in local direction of motion between object and background (Royden and Connors, 2010). Humans can also detect object motion based on local differences in speed when there are sufficient depth cues (Rushton et al., 2007; Royden et al., 2016) or when the image speed of an object is outside the range of background speeds in a particular task context (Royden and Moore, 2012).

Royden and Holloway, 2014 have shown that a model built on MT-like operators with surround suppression can effectively detect object motion when there are sufficient directional differences between object and background motion, or when object speed is outside the range of background speeds. However, such a model would not be able to detect object motion under task conditions like ours or those of Rushton et al., 2007, because our dynamic object had the same motion axis as the stationary distractors and because the speeds of our dynamic objects were well within the range of speeds of stationary objects. More recently, Royden et al., 2015 have added disparity-tuned operators to their model, which allow detection of object motion even when it is aligned with background flow lines. This model computes local differences in response of separate velocity and disparity-tuned operators. It then applies an arbitrary threshold to detect cases for which there are differences and identifies these as possible object motion. While this model shows that differences in signals related to motion and disparity can be used to identify object motion in more general cases, it does not provide a biologically plausible neural mechanism.

Our findings demonstrate a key, and apparently thus far unappreciated, neural mechanism for identifying local discrepancies between binocular disparity and motion parallax cues that accompany moving objects, even in difficult cases for which there are no local differences in the direction or timing of image motion. The activity of MT neurons with incongruent depth tuning for motion parallax and disparity provides a critical signal about these local discrepancies. Moreover, our simulations indicate that these signals can be easily read out by a linear decoder to detect object motion during self-motion.

A more general approach to computing scene-relative object motion during self-motion is flow parsing, in which global patterns of background motion related to self-motion are discounted (i.e. subtracted off) such that the remaining signal represents object motion relative to the scene (Rushton and Warren, 2005). Several studies Warren and Rushton, 2007; Warren and Rushton, 2008; Warren and Rushton, 2009a; Warren et al., 2012; Foulkes et al., 2013; Rushton et al., 2018 have provided strong behavioral support for the flow-parsing hypothesis in humans, including some which suggest strongly that it involves a global motion process (Warren and Rushton, 2009b). In addition, a recent study has demonstrated flow parsing in macaque monkeys (Peltier et al., 2020). If flow parsing completely discounts background motion due to self-motion, then the computations for detecting scene-relative object motion would be greatly simplified and would be essentially the same as when there is no self-motion. However, flow parsing alone may not be sufficient to detect scene-relative object motion. Recent evidence (Niehorster and Li, 2017; Peltier et al., 2020) indicates that the gain of flow parsing can be well below unity, such that background motion is only partially discounted. In this case, the output of a flow-parsing mechanism may not be sufficient to detect scene-relative object motion, and a mechanism such as we found in area MT would be valuable.

An advantage of our proposed mechanism over flow parsing is that it does not require estimation of the global flow field, nor a complicated mechanism (Layton and Fajen, 2016b; Layton and Fajen, 2020) for implementing the flow-parsing computation at each location in the visual field. Thus, our proposed mechanism may provide a valuable complement to flow parsing. On the other hand, the mechanism that we have described clearly does not obviate the need for flow-parsing mechanisms. Unlike our local mechanism, flow parsing does not require binocular disparity signals to operate. Furthermore, flow parsing allows for the estimation of scene-relative object velocity, rather than just facilitating object motion detection. Thus, our results do not discount the contributions of center-surround or flow-parsing mechanisms to computation of object motion, nor the contributions of mechanisms that may rely on multisensory signals (Kim et al., 2016b). Rather, our findings provide evidence of an additional complementary mechanism that is likely to be synergistic. Indeed, since our stimuli involved peripheral background dots (Figure 1—figure supplement 1A), it is possible that our task also engaged flow-parsing mechanisms to some extent.

We have recently demonstrated flow parsing in macaque monkeys (Peltier et al., 2020), including the observation that optic flow in one visual hemi-field can influence perception of object direction in the opposite hemi-field, as demonstrated previously in humans (Warren and Rushton, 2009b). These observations imply a global contribution to flow parsing, as might be implemented through feedback from the dorsal subdivision of the medial superior temporal area (MSTd) (Layton and Fajen, 2016b; Layton and Fajen, 2020). Indeed, in ongoing work, we have observed that flow parsing modulates responses of MT neurons (unpublished). In contrast, the mechanism described here can be computed locally within each portion of the visual field. Thus, we can speculate that the current findings and flow parsing involve distinct neural mechanisms in area MT.

Our findings establish the first direct (albeit correlational) evidence for a neural mechanism that is involved in perceptual dissociation of object and self-motion. However, the broader problem is more complex, as it is also necessary to flexibly compensate for self-motion to compute object motion in different coordinate frames, such as head-centered or world-centered reference frames (Fajen et al., 2013; Sasaki et al., 2020). Some of these computations are likely to also rely on non-visual signals including vestibular signals about self-motion (Fajen and Matthis, 2013; Fajen et al., 2013; Dokka et al., 2015a; Dokka et al., 2015b; Sasaki et al., 2017; Dokka et al., 2019; Sasaki et al., 2020). Thus, the mechanism proposed here is one part of a larger set of neural computations that remain to be fully understood.

Area MT has traditionally been considered to hold a retinotopic representation of retinal image motion. Many studies still make this assumption, despite the fact that MT is known to be modulated by attention (Treue and Maunsell, 1996; Treue and Maunsell, 1999; Martínez-Trujillo and Treue, 2002; Womelsdorf et al., 2008; Lee and Maunsell, 2010), eye movements (Newsome et al., 1988; Bremmer et al., 1997; Inaba et al., 2007; Chukoskie and Movshon, 2009; Nadler et al., 2009; Inaba et al., 2011; Kim et al., 2017), and stimulus expectation (Schlack and Albright, 2007). Our previous work has shown that MT neurons integrate retinal image motion with smooth eye movement (Nadler et al., 2008; Nadler et al., 2009) and global background motion (Kim et al., 2015a) signals to compute depth from motion parallax. In addition, most MT neurons are well known to be tuned for binocular disparity (Maunsell and Van Essen, 1983; DeAngelis and Newsome, 1999; DeAngelis and Uka, 2003). Recent studies (Nadler et al., 2013; Kim et al., 2015a) revealed the existence of many MT neurons that have mismatched depth tuning for motion parallax and binocular disparity cues. Such neurons would presumably not be useful for cue integration in depth perception, and their functional role has thus far remained unclear. In the present study, we demonstrate that such ‘opposite’ neurons provide valuable signals for detecting object motion during self-motion by selectively responding to local inconsistencies between binocular disparity and motion parallax cues. Thus, our findings provide novel evidence that the functional roles of MT go well beyond representing retinal image motion; they suggest that some MT neurons play fundamental roles in helping to infer the origins, or causes, of retinal image motion.

Our findings have parallels to the potential function of neurons in area MSTd and the ventral intraparietal (VIP) area that have mismatched heading tuning for visual and vestibular cues (Gu et al., 2006; Gu et al., 2008; Chen et al., 2011; Chen et al., 2013). Studies of cue integration and cue re-weighting in heading perception have demonstrated that activity of congruent cells can account for behavioral performance (Gu et al., 2008; Fetsch et al., 2011), but the functional role of opposite cells remained unclear from those studies. More recent work has suggested that opposite neurons may play a role in helping parse the retinal image into signals related to self-motion and object motion (Kim et al., 2016b; Sasaki et al., 2017), although they did not link opposite cell activity to a relevant behavior. Thus, mismatched tuning, whether unisensory or multisensory, may be a common motif for performing computations that involve parsing sensory signals into components that reflect different causes in the world (Zhang et al., 2019a).

More generally, the parsing of retinal image motion into components related to object motion and self-motion is a causal inference problem (Körding et al., 2007; Shams and Beierholm, 2010; French and DeAngelis, 2020), and recent psychophysical work in humans has demonstrated that perception of heading in the presence of object motion follows predictions of a Bayesian causal inference model (Dokka et al., 2019). While the neural mechanisms of causal inference are still largely unknown (but see Fang et al., 2019), recent computational work has suggested that the relative activity of congruent and opposite cells may provide a critical signal for carrying out causal inference operations (Zhang et al., 2019b; Rideaux et al., 2021). By providing an empirical link between the activity of opposite cells and detection of object motion during self-motion, our results provide novel evidence for a sensory substrate that may be used to perform causal inference in the domain of object motion and self-motion perception. Elucidating the neural substrates and mechanisms of causal inference regarding object motion is the topic of ongoing studies in our laboratories.

Two male monkeys (macaca mulatta, 8–12 kg) participated in these experiments. Standard aseptic surgical procedures under gas anesthesia were performed to implant a head restraint device. A Delrin (Dupont) ring was attached to the skull using a combination of dental acrylic, bone screws, and titanium inverted T-bolts (see Gu et al., 2006 for details). To monitor eye movements using the magnetic search coil technique, a scleral coil was implanted under the conjunctiva of one eye.

A recording grid made of Delrin was affixed inside the ring using dental acrylic. The grid (2×4×0.5 cm) contains a dense array of holes spaced 0.8 mm apart. Under anesthesia and using sterile technique, small burr holes (~0.5 mm diameter) were drilled vertically through the recording grid to allow the penetration of microelectrodes into the brain via a transdural guide tube. All surgical procedures and experimental protocols were approved by University Committee on Animal Resources at the University of Rochester.

In each experimental session, animals were seated in a custom-built primate chair that was secured to a six degree-of-freedom motion platform (MOOG 6DOF2000E). The motion platform was used to generate passive body translation along an axis in the fronto-parallel plane, and the trajectory of the platform was controlled in real time at 60 Hz over a dedicated Ethernet link (see Gu et al., 2006 for details). A field coil frame (C-N-C engineering) was mounted on top of the motion platform to measure eye movements.

Visual stimuli were rear-projected onto a 60×60 cm tangent screen using a stereoscopic projector (Christie Digital Mirage S+3 K) which was also mounted on the motion platform (Gu et al., 2006). The display screen was attached to the front side of the field coil frame. To restrict the animal’s field of view to visual stimuli displayed on the tangent screen, the sides and top of the field coil frame were covered with matte black enclosures. Viewed from a distance of ~30 cm, the display subtended ~90°×90° of visual angle.

To generate accurate visual simulations of the animal’s movement through a virtual environment, an OpenGL camera was placed at the location of one eye, and the camera moved precisely according to the movement trajectory of the platform. Since the motion platform has its own dynamics, we characterized the transfer function of the motion platform, as described previously (Gu et al., 2006), and we generated visual stimuli according to the predicted motion of the platform. To account for a delay between the command signal and the actual movement of the platform, we adjusted a delay parameter to synchronize visual motion with platform movement. Synchronization was confirmed by presenting a world-fixed target in the virtual environment and superimposing a small spot by a room-mounted laser pointer while the platform is in motion (Gu et al., 2006).

We recorded extracellular single unit activity using single-contact tungsten microelectrodes (FHC Inc) having a typical impedance of 1–3 MΩ. The electrode was loaded into a transdural guide tube and was manipulated with a hydraulic micro-manipulator (Narishige). The voltage signal was amplified and filtered (1 kHz–6 kHz) using conventional hardware (BAK Electronics). Single unit spikes were detected using a window discriminator (BAK Electronics), whose output was time stamped with 1 ms resolution.

Eye position signals were digitized at 1 kHz, then digitally filtered and down sampled to 200 Hz (TEMPO, Reflective Computing). The raw voltage signal from the microelectrode was digitized and recorded to disk at 25 kHz using a Power1401 data acquisition system (Cambridge Electronic Design). If necessary, single units were re-sorted off-line using a template-based method (Spike2, Cambridge Electronic Design).

The location of area MT was initially identified in each animal through analysis of structural MRI scans, which were segmented, flattened, and registered with a standard macaque atlas using CARET software (Van Essen et al., 2001). The position of area MT in the posterior bank of the superior temporal sulcus (STS) was then projected onto the horizontal plane, and grid holes around the projection area were explored systematically in mapping experiments. In addition to the MRI scans, the physiological properties of neurons and the patterns of gray matter and white matter encountered along electrode penetrations provided essential evidence for identifying MT. In a typical electrode penetration through the STS that encounters area MT, we first encounter neurons with large RFs and visual motion sensitivity (as expected for area MSTd). This is typically followed by a very quiet region as the electrode passes through the lumen of the STS, and then area MT is the next region of gray matter. As expected from previous studies, RFs of MT neurons are much smaller than those in MSTd (Komatsu and Wurtz, 1988) and some MT neurons exhibit strong surround suppression (DeAngelis and Uka, 2003) which is typically not seen in MSTd. Confirming a putative localization of the electrode to MT, we observed gradual changes in the preferred direction, preferred disparity, and RF location of multiunit activity, consistent with those described previously (Albright et al., 1984; DeAngelis and Newsome, 1999).

Visual stimuli were generated by a custom-written C++ program using the OpenGL 3D graphics library (Kim, 2013, https://github.com/hkim09/MoogDots_2013) and were displayed using a hardware-accelerated OpenGL graphics card (NVIDIA Quadro FX 1700). The location of the OpenGL camera was matched to the location of the animal’s eye, and images were generated using perspective projection. We calibrated the display such that the virtual environment had the same spatial scale as the physical space through which the platform moved the animal. To view stimuli stereoscopically, animals wore anaglyphic glasses with red and green filters (Kodak Wratten 2 Nos. 29 and 61, respectively). The crosstalk between eyes was measured using a photometer and found to be very small (0.3% for the green filter and 0.1% for the red filter).

Although the object detection task is conceptually simple, it required extensive behavioral training, involving a number of steps. Here, we outline a series of operant conditioning steps required to teach animals to perform the task. Following basic chair training and habituation to the laboratory, animals were trained to maintain visual fixation on a target during sinusoidal translation of the motion platform.

Once smooth eye movements tracked the fixation target with pursuit gains approaching 0.9, we initially trained animals to detect a moving object without any self-motion, such that any motion of an object on the display resulted from object motion relative to the scene. After fixation, four objects appeared on the display and only one of them moved sinusoidally along a horizontal trajectory for 2.1 s. In the early stages of this training, a saccade target appeared only at the location of the moving object. Subsequently, we introduced a fraction of trials in which saccade targets appeared at the locations of all four objects, and we gradually increased the proportion of these trials. During this phase of training, the depths of the objects, as defined solely by binocular disparity since there was no self-motion, were randomly drawn from a uniform distribution spanning the range from –1.6 to +1.6 deg, to help animals generalize the task.

Once animals performed the task well in the absence of self-motion, we began to introduce small amounts of sinusoidal self-motion, which induced subtle retinal image motion of all objects. During the initial stages of this training period, the dynamic object had a large motion amplitude such that it was quite salient relative to the motion of stationary objects that was due to self-motion. As the animals became accustomed to performing the task during self-motion, we gradually increased the magnitude of self-motion (up to 2.8 cm) and decreased the motion amplitude of the dynamic object. Once the retinal motion amplitude of the dynamic object became comparable to that of stationary objects, we began to introduce a depth discrepancy between disparity and motion parallax (ΔDepth). That is, the motion trajectory of the dynamic object began to follow that of an object at a different depth, d_MP (Figure 1—figure supplement 1B, right). We used a staircase procedure to train animals over a range of values of ΔDepth. During this phase of training, we interleaved three different pedestal depths (–0.51 deg, 0 deg, and 0.51 deg) to help animals generalize the task, and we randomly chose the depths of the three stationary objects from the range –1.6 to +1.6 deg.

Once we observed stable ‘v-shaped’ psychometric functions for all three pedestal depths over a span of more than 10 days (e.g. Figure 1—figure supplement 3A, B), we transitioned to the final stimulus configuration for recording experiments. To keep the number of stimulus conditions manageable for recording, this configuration included one pedestal depth and two objects (one dynamic and one stationary). Following recording experiments, we revisited the more general version of the task involving four objects and three pedestal depths to make sure that behavioral performance did not reflect any change in strategy (e.g. Figure 1—figure supplement 3C).

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

We thank Johnny Wen for programming assistance, as well as Swati Shimpi, Emily Murphy, and Dina Graf for assistance with training animals. This work was supported by NEI R01 grant EY013644, NINDS U19 grant NS118246, and by an NEI Core grant (EY001319).

All surgical procedures and experimental protocols were approved by the University Committee on Animal Resources at the University of Rochester (#100682) and were performed in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health.

© 2022, Kim et al.

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.