An intriguing property of the visual system is how easily and effortlessly we perceive objects (sensory processing), and discriminate among those of similar appearance, even when the particular exemplar has never been seen before. We quickly distinguish any red tomato from any red apple, regardless of the variety. A half-century of behavioral, anatomical and physiological research has revealed that this feat of visual perception is supported by a sequence of connected brain regions stretching from the occipital cortex to inferior temporal cortex (Figure 1A) (Gross et al., 1972; Ungerleider and Mishkin, 1982). Simple features, such as oriented edges or lines, are represented in caudal regions, beginning with area V1 (Hubel and Wiesel, 1959). Conjunctions of features defining whole objects are represented in rostral regions, culminating with area TE (Kobatake and Tanaka, 1994). Directly adjacent to area TE is rhinal cortex, an anatomically distinct region that receives dense projections from area TE (Suzuki and Amaral, 1994), and is thought to be important primarily for memory function (Meunier et al., 1993; Higuchi and Miyashita, 1996). It has more recently been suggested that rhinal cortex is important for visual perception of complex objects or objects with over-lapping features, and hence might be considered the final stage of the visual perceptual processing hierarchy (Buckley et al., 2001; Bussey et al., 2003; Baxter, 2009), but see Hampton, 2005, Suzuki (2009).

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To determine whether visual object processing is finalized in area TE, or whether it extends to rhinal cortex, categorization was tested at several levels of perceptual difficulty in a series of experiments using stimuli with overlapping features. All tasks required remembering visual perceptual categories. However, in every trial, the monkeys responded while the stimulus was present, thereby minimizing demands on short-term memory.

We tested three groups of three monkeys: an unoperated control group, a group with a bilateral removal of area TE, and a group with a bilateral removal of rhinal cortex (including peri- and ento- rhinal cortex). Monkeys were trained to perform a cat vs. dog category discrimination in a visually cued two-interval forced choice (2-IFC) paradigm (Figure 1B) (Matsumoto et al., 2016). They were required to judge whether an image was more dog-like or cat-like when presented with stimuli drawn from a set of category-ambiguous ‘morphed’ images, created by blending and warping cats with dogs in different proportions. The monkeys responded while a stimulus was present, thereby minimizing demands on short-term memory.

Experiment 1 – learning to categorize morphed stimuli

In Experiment 1, monkeys were presented with a set of stimuli comprising cats, dogs, and intermediate morphed images spaced at 10% increments on an arbitrary scale (Abrosoft, Beijing, China) from 0 % to 100% dog (Figure 1C). Monkeys could avoid an extended inter-trial delay by releasing the bar in the first interval (signaled by a red target) for stimuli that were less than 50% dog, and were rewarded for releasing the bar in the second interval (signaled by a green target) for stimuli that were more than 50% dog. This amounts to an asymmetrical reward structure. They were rewarded randomly for releasing during the green interval for 50 – 50 morphs. The monkeys in all three groups classified most stimuli well the first time they were presented (Figure 2A,B,C). The control and rhinal-removal groups improved quickly with repetition, reaching asymptotic performance by the 10th repeat of the stimulus set (Figure 2D). The TE-removal group was slower to learn, only reaching the level of performance of controls by the 14th repetition of the stimulus set. Across presentations, the group with TE removals categorized less accurately than the control group (Linear Mixed Effects model, LME, p=0.0072, z = 2.69). The deficit seen in the TE-removal group might be attributable to slower learning, as there was an interaction effect between number of presentations by treatment group (Ctl vs. TE) by morph level (LME, p=1.07×10⁻⁸, z = −5.72). The performance of the group with rhinal removals was indistinguishable from that of controls (LME, p=0.23, z = −1.19).

Figure 2

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Experiment 1 - learning to categorize morphed images.

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Experiment 2 – area TE removal impairs perceptually difficult categorization

In Experiment 2, we examined sensitivity to perceptual ambiguity at the category boundary, where classification should be most difficult. The stimuli used in Experiment 2 were derived from the same cat and dog pairs used in Experiment 1. We continued to explore the full range of category space (from 0% to 100% dog), but biased the distribution of stimuli towards the category boundary (cat 50:50 dog) by presenting stimuli consisting of the following ratios of cat:dog: 100:0, 75:25, 65:35, 60:40, 55:45, 50:50, 45:55, 40:60, 35:65, 25:75, and 0:100 (supplementary Figure 1). The asymmetrical reward structure of the task design produced a bias in all treatment groups toward classifying ambiguous stimuli as dogs, that is at the 50% morph level an unbiased subject would report the stimuli as dog-like 50% of the time. However, control monkeys reported the 50:50 morphs as more dog-like on 70% of presentations. The rhinal-lesioned group showed a similar bias, reporting 64% as more dog-like. The TE-lesioned group showed a bias in the same direction as the other two groups, reporting 50:50 morphs as more dog-like 61% of the time. For this experiment, we are interested in the ability to categorize visual stimuli accurately which is measured by the steepness of the discrimination curve. To remove the confound of learning rate, and focus on perceptual processing, we continued testing the three different treatment groups until performance reached asymptotic levels. For Experiment 2, all groups had reached asymptotic performance by the tenth presentation of the stimuli. During presentations 11 to 20, the categorization accuracy of monkeys with bilateral aspiration removals of rhinal cortex was indistinguishable from that of controls (LME, p=0.49, z = −0.68). Monkeys with bilateral TE removals made significantly more incorrect assignments than the other two groups (LME, p=2.64×10⁻¹⁰, z = −6.32), but nonetheless categorized better than would be expected by chance (t test, p=0.00057, d.f. = 5, t = −7.49) (Figure 3A). It seems unlikely that the impairment in making visual category discriminations following TE removals could be attributed to a learning deficit, because performance of all three test groups was stable throughout the latter 10 presentations of the test stimuli (LME, effect of repetition, p=0.54, z = −0.61).

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Experiment 2 - asymptotic categorization performance.

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For all monkeys, the closer the stimulus was to the category boundary, the longer it took to release the lever on correct trials during the presence of the red target (LME – effect of morph level, p=0.0017, d.f. = 5, t = 5.23) (Figure 3B,C,D), supporting the inference that classification is more difficult near the category boundary. The latency to release following the green target was constant across difficulty levels because the monkeys had presumably made the decision that the stimulus was dog-like earlier in the trial (LME – effect of morph level, p=0.40, d.f. = 5, t = 0.26). We interpret the response time to the green target as the basic visual-motor reaction time. Reaction times did not differ across groups, suggesting that TE removal did not slow the decision process (reaction times during red target (LME, p=0.15, d.f. = 2, t = 1.35)), nor did it slow the basic visual-motor reaction time (reaction time during green target (LME, p=0.48, d.f. = 2, t = −0.069)). The deficits observed in the TE group are also unlikely to be due to a failure in basic visual acuity, because grating contrast-sensitivity – a test designed to assess the visual acuity of human subjects (Blakemore and Campbell, 1969) - was indistinguishable across all three groups (Ctl vs TE: LME, p=0.28, d.f. = 2, t = −0.69; Ctl vs Rh: LME, p=0.22, d.f. = 2, t = −0.95)) (Figure 4), and similar to those of humans (Blakemore and Campbell, 1969).

Figure 4

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Visual acuity testing.

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Motivation and attention did not seem to be altered in either lesion group because the reaction times of all groups were indistinguishable, and there were few late bar release errors (<1% on average) – the few late release errors that were recorded were not distributed significantly differently among the treatment groups (Kruskal-Wallis, χ² = 2.49, p=0.29).

Experiment 3 – area TE impairment with visually degraded stimuli

Experiment 3 tested the possibility that monkeys with large cortical removals (TE/rhinal) had compensated for a deficit in object perception/categorization by memorizing one or more simple diagnostic features of each morph series (e.g. the ‘tail’ of the stimuli in the second row of Figure 1C). It has been demonstrated previously that the performance of monkeys with perirhinal cortex lesions is indistinguishable from controls in discriminating perceptually dissimilar stimuli obscured by masks (Hampton and Murray, 2002). The rationale for using the approach here, with perceptually similar stimuli, was if the monkeys were relying on a single diagnostic feature of the morphed stimuli to establish category membership in Experiment 2, image degradation of this nature (Figure 5A) would have a detrimental effect on performance. Consistent with this hypothesis, monkeys with bilateral TE removals were severely impaired by the masks relative to their own overall performance in the inter-leaved unmasked trials (Figure 5D) (LME, p=2×10⁻¹⁶, z = 9.03). They categorized the masked stimuli significantly less accurately than controls (Figure 5B) (LME, p=0.0017, z = 3.13). The performance of controls and that of monkeys with rhinal removals was indistinguishable (LME, p=0.20, z = −1.27); both groups exhibited smaller reductions in classification accuracy than the TE group in the presence of the masks, relative to the inter-leaved unmasked trials (Figure 5C,E) (Ctl: LME, p=8.92×10⁻¹¹, z = 6.48; rhinal: LME, p=1.33×10⁻¹⁰, z = 6.42). Due to the asymmetrical reward structure of this and similar tasks, when monkeys fail to discriminate between the two offers they will usually resort to releasing the lever during the presence of the green target 100% of the time, as this is the only condition in which reward is available. This bias is visible in the impaired performance of the TE-lesioned monkeys following the foreground masking of the stimuli performed in Experiment 3.

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Experiment 3 - categorization of visually degraded stimuli.

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Experiment 4 – area TE impairment with a novel stimulus set

In Experiment 4, a large set of novel morphs were used as trial-unique stimuli in a single session to control for the possibility that the monkeys memorized individual stimulus-response outcomes in Experiments 1, 2 and 3. It has been demonstrated that visual discrimination of complex stimuli can be performed independently of area TE and of rhinal cortex if the stimuli have become sufficiently well learned (Eacott et al., 1994). We morphed a set of cat images each with two dog images, and vice versa (Figure 6A, supplementary Figure 2). This manipulation reduces the utility of a strategy focused on a single memorized feature (e.g. in Figure 4A, note the difference in appearance of the tail of ‘Cat A’ at the 50% morph level when paired with ‘Dog A’, versus the 50% level when paired with ‘Dog B’). Consistent with the results of Experiment 3, monkeys lacking area TE categorized stimuli significantly less accurately than controls (LME, p=2×10⁻¹⁶, z = 9.18), whereas those with rhinal cortex removals were indistinguishable from controls (Figure 6B) (LME, p=−0.62, z = −0.50).

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Experiment 4 - categorization of novel stimuli.

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According to the hierarchical model of object perception, area TE plays an important role in the integration of visual features into identifiable objects. The results from the experiments described above suggest that area TE is only important for perceiving and classifying objects with complex over-lapping features, especially when novel/unfamiliar. The monkeys with TE removals were surprisingly good at classifying all but the most ambiguous stimuli (i.e. those closest to the category boundary). Perception of simple, low-level features appears to be intact in the monkeys lacking TE as shown by their normal ability to detect the change in color of the target from red to green in Experiments 1 – 4, and by their normal contrast sensitivity when tested with black and white sine wave gratings.

There is a debate in both human and non-human primate literature about whether medial temporal lobe tissue - rhinal cortex - is important for the perception of feature-ambiguous stimuli (Lee et al., 2005; Levy et al., 2005; Buckley and Gaffan, 2006; Baxter, 2009; Suzuki, 2009; Lee and Rudebeck, 2010). The proposal that the visual object processing hierarchy includes perirhinal cortex arose from studies claiming a role for monkey perirhinal cortex in visual perception following tests of visual discrimination, oddity detection, or delayed-match-to-sample (DMS) at zero delay (Eacott et al., 1994; Buckley et al., 2001; Bussey et al., 2003). The aforementioned tasks required monkeys to compare an image with one or more specific images that must be maintained in memory (even in the case of the oddity task – in which stimuli appear simultaneously – the subject must maintain a representation of two or more features from three or more images to make a correct choice, a process that presumably requires the subjects to look at each image in turn and remember those already looked at). In ‘delayed matching’ tasks, monkeys with removals of rhinal cortex are only impaired when there is a delay of several seconds between the sample and test stimuli (Buffalo et al., 1999), and have impaired short-term memory but intact habit formation for the exact same images (Tu et al., 2011). In the present study, monkeys that had received lesions several years prior to testing (and hence compensatory reorganization in response to the testing series is unlikely) performed a task which only requires memory for a categorical exemplar or boundary, along with the category-response mapping. The anatomical extent of the rhinal removals was comparable to those described in the above-mentioned studies. Nonetheless, performance of rhinal-lesioned monkeys was indistinguishable from that of control monkeys by all measures. It could be argued that because categorization tasks require generalization across perceptually similar stimuli, that such tasks may be solved using features of intermediate complexity, rather than gestalt object representations (the latter being the type of perceptual function some have tried to ascribe to rhinal cortex (Bussey et al., 2003)). Although we cannot preclude this possibility, the large degree of feature overlap in our stimulus sets (c.f. the 40% vs. 60% morphed stimuli in Figure 1C) means that there are no obvious such intermediate features on which the task could be solved. When the discriminations are made more difficult (Experiments 3 and 4), there are no large changes in the response selections of the control and rhinal-lesioned groups. However, there are two changes in the response patterns of the TE-lesioned monkeys; first, their discrimination performance becomes considerably worse as shown by the decrease in slope of the discrimination curve. Second, the monkeys have changed their criterion for classifying a stimulus as a dog as shown by the shift in the 50% discrimination point to the left. Since these changes occur when the discrimination is made difficult, we can conclude that the monkeys have a discrimination deficit, and in the face of the discrimination being made more difficult the monkeys have changed their criterion by classifying more trials as dogs. The change in criterion is not surprising in the face of the asymmetrical reward structure of the task. The most parsimonious interpretation of these observations is that monkeys assess each image in its entirety in order to make a categorical judgement, and hence it seems that the TE-rhinal boundary represents the end of perceptual processing in the ventral visual stream.

The lack of evidence for a role of rhinal cortex in perceptual processing reported here suggests that previous reports of deficits in visually guided behavior following rhinal removals may be attributable to memory deficits. This interpretation is supported by a number of studies demonstrating a role for rhinal cortex in mnemonic processes. In behavioral testing, monkeys lacking rhinal cortex are impaired in object recognition (Meunier et al., 1993), and learning stimulus-stimulus associations (Murray et al., 1993). They are also severely impaired in comparing reward values across time (Liu et al., 2000), even when vision plays no role in the task (Clark et al., 2012). Rhinal cortex neurons appear to be tuned for complex stimuli in a similar manner to those recorded in area TE. However, neuronal responses in TE generally exhibit task-invariant tuning for specific stimuli (McMahon et al., 2014), whereas neuronal responses in rhinal cortex are modulated by behavioral context (Yakovlev et al., 1998; Lehky and Tanaka, 2007; Naya and Suzuki, 2011; Eradath et al., 2015). For example, when the stimulus-mapping in a delay-discounting task is randomized, perirhinal neurons lose their selectivity on the next trial (Liu and Richmond, 2000). The loss of stimulus selectivity in perirhinal neurons following a contextual change implies that the apparent selectivity is derived from a learned association with predicted outcome.

Rhinal cortex neurons are also sensitive to learned stimulus-stimulus associations; they form a functional microcircuit that is dynamically modulated by task demand (Erickson and Desimone, 1999; Hirabayashi et al., 2013) and they convey information relevant to behavioral choice in a more accessible manner than those in TE (Pagan et al., 2013; Pagan and Rust, 2014). Furthermore, the delay between TE and perirhinal neural responses to visual stimuli is considerably longer (~60 ms) than is usually attributed to a direct feed-forward mechanism (10–15 ms) (Xiang and Brown, 1998; Liu and Richmond, 2000); this suggests that rhinal cortex is doing more than a simple monosynaptic transformation of visual input from TE neurons. In the current study, a variety of manipulations that increased the perceptual difficulty of a categorization task revealed significant, although far from catastrophic, deficits in monkeys with bilateral TE removals, and no deficits in monkeys with bilateral rhinal removals. Thus, the final stage of image processing in the ventral visual stream appears to occur in area TE. Rhinal cortex is critical for learning and remembering contextual or associative relations among stimuli or events, but appears to play no role in object percept formation.

All data generated or analysed during this study are included in the manuscript and supporting files.

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Author details

1. Mark AG Eldridge

   Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, United States

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Supervision, Validation, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   mark.a.g.eldridge@gmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4292-6832

2. Narihisa Matsumoto

   Human Informatics Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Japan

   Contribution

   Conceptualization, Software, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

3. John H Wittig Jnr

   Surgical Neurology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, United States

   Contribution

   Conceptualization, Resources, Data curation, Software, Supervision, Investigation, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0465-1022

4. Evan C Masseau

   Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, United States

   Contribution

   Conceptualization, Resources, Data curation, Software, Investigation, Methodology, Project administration

   Competing interests

   No competing interests declared

5. Richard C Saunders

   Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, United States

   Contribution

   Conceptualization, Resources, Formal analysis, Supervision, Funding acquisition, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

6. Barry J Richmond

   Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, United States

   Contribution

   Conceptualization, Resources, Data curation, Software, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   barry.richmond@nih.gov

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-8234-1540

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