Our understanding of the sensory systems and behavior of animals is challenging to contextualize within the framework of evolution. Anatomical comparisons between species have allowed us to infer sensory capabilities, but this approach cannot directly reveal neural function. Discovery of neural mechanisms that underlie behavior are often constrained to a limited number of model species (Jourjine and Hoekstra, 2021). Like morphology, neural circuits can adapt to the environment. Of these, many circuits are sensory and regulate essential behaviors such as foraging, navigation, and escapes (Blin et al., 2018; Hoke et al., 2012; Hüppop, 1987; Paz et al., 2020).

The Mexican blind cavefish, Astyanax mexicanus, is a powerful model to understand the evolution of physiological and molecular traits that contribute to behaviors such as sleep (Duboué et al., 2011; Jaggard et al., 2018) and prey capture (Lloyd et al., 2018; Yoshizawa et al., 2014). A. mexicanus exists in two morphs: (1) eyed surface-dwelling populations and (2) blind cave populations. There are at least 30 independently evolved cavefish populations in the caves of the Sierra de El Abra region of Northeast Mexico (Espinasa et al., 2018; Herman et al., 2018; McGaugh et al., 2020; Mitchell et al., 1997). A. mexicanus populations are interfertile, and this attribute has allowed investigators to demonstrate independent convergence of numerous behavioral, developmental, and physiological traits (Chin et al., 2018; Kowalko, 2020; Riddle et al., 2018; Stockdale et al., 2018; Varatharasan et al., 2009). Our goal is to apply a neurophysiological approach across multiple A. mexicanus populations to examine the functional evolution of the lateral line sensory system.

The mechanoreceptive hair cells of the lateral line system detects fluid motion relative to the body and play an important role in essential behaviors (McHenry et al., 2009; Mekdara et al., 2018; Olszewski et al., 2012; Oteiza et al., 2017; Stewart et al., 2013). Cavefish have evolved anatomical enhancements of the lateral line, presumably to compensate for the loss of vision (Kowalko, 2020; McGaugh et al., 2020; Teyke, 1990; Yoshizawa et al., 2012). These anatomical alterations have been linked to substantial changes in behavior (Lloyd et al., 2018; Yoshizawa et al., 2010). However, almost nothing is known about physiological changes that accompany evolution, despite the fact that the response of peripheral senses to environmental change has been well documented (Kelley et al., 2018; McBride, 2007).

Endogenous depolarizations within sensory cells are transmitted to afferent neurons (hereafter ‘afferents’) as spontaneous action potentials (hereafter ‘spikes’), and are essential for maintaining a state of responsiveness and sensitivity (Kiang, 1965; Manley and Robertson, 1976). For example, the spontaneous spikes from auditory hair cells have been shown to enable precise encoding of much higher frequencies (Köppl, 1997). Here, we suggest a similar underlying mechanism, though the correlation of spontaneous activity to sensitivity in the lateral line awaits empirical evidence. In the lateral line, spontaneous depolarizing currents within the hair cell maintain a resting potential within the critical activation range of channels. This range is required to ensure transmitter release; thus these currents decrease the detection threshold of the system (Trapani and Nicolson, 2011). Spontaneous afferent activity is an established and reliable target for probing the neurophysiological basis of sensitivity across taxa (Hedwig, 2006; Krasne and Bryan, 1973; Mohr et al., 2003). Here, we use spontaneous afferent activity as an entry point into understanding the neural mechanism underlying lateral line function in cavefish.

Another important mechanism that determines lateral line sensitivity is an inhibitory feedback effect of the efferent system during swimming. Feedback mechanisms in general sculpt sensory systems in important ways; for example, by changing detection thresholds by altering the transmission frequency of afferent spikes (Crapse and Sommer, 2008; Straka et al., 2018). The efferent system of hair cells in particular has repeatedly evolved to modulate sensory processing (Köppl, 2011). More specifically, hindbrain efferent neurons (hereafter ‘efferents’) issue predictive signals that transmit in parallel to locomotor commands, termed corollary discharge (CD). CDs inhibit afferent activity to mitigate sensor fatigue that can result from self-generated stimuli (Russell and Roberts, 1972). CD is an important mechanism for sensitivity enhancement but has rarely been implicated for ecologically relevant behaviors. For example, active-flow sensing by cavefish depends on detecting reafferent signals while swimming (Tan et al., 2011). Increased reliance on self-generated fluid motion (Odstrcil et al., 2022; Patton et al., 2010; Teyke, 1985) is divergent from our current understanding of the CD’s role in predictive motor signaling in the lateral line (Lunsford et al., 2019; Pichler and Lagnado, 2020).

For the first time, we identify a neurophysiological mechanism that has convergently evolved across A. mexicanus populations to increase hair cell sensitivity after eye loss. By investigating how differences in afferent and efferent signaling contribute to sensory enhancement in a comparative model, we provide insight into a potentially ubiquitous mechanism for sensory evolution.

Neuromasts of surface fish and Pachón cavefish larvae (6 days post fertilization; dpf) were labeled via 2-[4-(dimethylamino)styryl]-1-ethylpyridinium iodide (DASPEI) staining and subsequently imaged (Figure 1B, C). Anterior lateral line (ALL) neuromasts had previously been shown to differ in quantities and morphology as early as 2 months post fertilization between surface and cavefish (Yoshizawa et al., 2010). Here, we show that Pachón cavefish exhibit this significant increase in anterior neuromast quantity as early as 6 dpf (p < 0.01, t = 3.168, df = 29; Figure 1D). In contrast, both populations exhibit a similar number of posterior lateral line neuromasts (p = 0.77, U = 111.5; Figure 1E). Neuromasts along the posterior lateral line were comprised of similar quantities of hair cells across blind (n = 11) and surface morphs (n = 9; p = 0.09; Figure 1F). No significant interaction was detected between the effects of population and age (5–7 dpf; F_2,72 = 2.96, p = 0.06; Figure 1G). We exclusively probed the posterior lateral line afferent neurons to establish whether sensory systems that are anatomically similar exhibit neurophysiological differences that contribute to enhanced sensitivity.

Figure 1

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To examine the physiological basis of differences in lateral line function across surface and cavefish we used extracellular lateral line recordings adapted from protocols used in zebrafish (Figure 2A, B). Extracellular recordings of posterior lateral line afferents revealed intrinsic spontaneous activity was higher in Pachón cavefish (18.6 ± 0.2 Hz) while the animal was at rest, relative to surface fish (12.4 ± 0.3 Hz; p < 0.01, t = 15.97, df = 5,795; Figure 2C). Single neuromasts were then deflected and evoked activity was recorded from the connected afferent neuron (Figure 2D, E). The neuromasts were stimulated at different frequencies (5–40 Hz) and a pairwise comparison of evoked afferent activity at 30 Hz revealed statistically elevated spike rates in Pachón cavefish (n = 12; 119.6 ± 16.6 Hz) relative to surface fish (n = 10; 73.2 ± 6.9 Hz; p = 0.03, t = 2.38, df = 18; Figure 2F). Significantly elevated spike rates were also detected in response to a 40-Hz stimulus in Pachón cavefish (101.3 ± 13.6 Hz) relative to surface fish (52.3 ± 7.0 Hz; p < 0.01, t = 3.00, df = 18; Figure 2F). Together these findings support spontaneous afferent activity as a reliable metric for estimating the sensitivity of the lateral line and reveal enhanced neural responses to hair cell deflection in cavefish.

Figure 2

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We examined afferent signaling during motor commands in our paralyzed preparation which were denoted by bouts of fictive swimming (hereafter swimming). Swim bouts of longer duration were observed in surface fish (357 ± 5 ms; n = 3167 swim bouts) when compared to Pachón cavefish (264 ± 4 ms; n = 2612 swim bouts; p < 0.01, t-stat = 15.2, df = 5777). Instantaneous afferent spike rate demonstrates substantial decreases during swimming in surface fish and little effect in Pachón cavefish (Figure 3A, B). We quantified and compared spike rates during swimming relative to the pre-swim period to examine patterns of the inhibitory effect between populations. During most surface fish swim bouts there was a reduction in afferent activity (n = 1966/2291, 85.8%), many of which resulted in complete quiescence of transmissions (n = 1112/2291, 48.5%). Conversely, afferent activity partially reduced during many swim bouts in Pachón cavefish (n = 1303/2439, 53.4%), but very few instances led to complete inhibition (n = 275/2439, 11.3%). The distributions of relative spike rates during swimming reveal surface fish have a higher likelihood of experiencing no afferent activity during swimming while cavefish experience afferent activity during swimming similar to that of pre-swim activity levels (Figure 3C). Therefore, surface fish experience significantly higher levels of inhibition (68.5 ± 0.01%) compared to cavefish (28.9 ± 0.01%; p < 0.01, t = 36.5, df = 4449; Figure 3D). Surface fish demonstrate lateral line inhibition during swimming comparable to other fishes with intact visual systems (Flock and Russell, 1973; Lunsford et al., 2019; Pichler and Lagnado, 2020; Russell and Roberts, 1972) suggesting cavefish have evolved a unique functional phenotype for sensory gain control.

Figure 3

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We imaged hindbrain cholinergic efferent neurons to determine anatomical and functional connectivity. Between populations, backfilled efferents revealed similar soma quantities (surface: 2.4±0.3; cave: 3.2±0.5; p = 0.2, t = 1.36, df = 18) and size (surface: 62.1 ± 3.6 µm²; cave: 70.9 ± 4.5 µm²; p = 0.1, t = 1.50, df = 51; Figure 4A–C). From electrophysiological recordings, we observed average spike rates during and prior to a swim were not positively correlated in control surface fish (r²=0.15, F_1,13 = 2.3, p = 0.2), but the slope of the line indicates a fractional suppression of 78% that is significantly less than unity (slope 0.1, confidence interval [CI]: −0.2 to 0.4; Figure 4Di). In the efferent-ablated surface fish, the spike rates during swimming intervals were indistinguishable from those during nonswimming intervals (slope 1.2, CI = −0.1 to 2.4) showing no detectable inhibitory effect. While swimming, surface fish without functioning efferent neurons demonstrated a signaling phenotype similar to both intact cavefish (slope 0.88, CI = −0.5 to 2.2) and cavefish with ablated efferents (slope 0.9, CI = 0.1 to 1.8; Figure 4Dii). Therefore, putative cholinergic hindbrain efferents are necessary for afferent inhibition in surface fish, but do not demonstrate modulatory control of afferents in cavefish.

Figure 4

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We compared pre-swim and swim spike rates across populations and treatments to determine efferent contribution to inhibition (Figure 4E). We found significant differences in afferent activity among pre-swim and swim intervals (F_7,40 = 7.6, p < 0.01; Figure 4F). Surface fish afferent spike rates during swimming (3.9 ± 0.1 Hz) were 71% lower than the immediate pre-swim period in control fish (13.7 ± 0.2 Hz; Tukey’s post hoc test, p < 0.01). Post-swim spike rate (13. 7 ± 0.3 Hz) recovered to pre-swim spike rate. In control Pachón cavefish, we observed some decrease in afferent spike rate during swimming (16.8 ± 0.2 Hz) but it was not statistically discriminated from pre-swim (20.5 ± 0.2 Hz; Tukey’s post hoc test, p = 0.94). Efferent ablation in surface fish resulted in afferent activity during swimming (17.4 ± 0.3 Hz) to increase to pre-swim levels (20.7 ± 0.3 Hz; Tukey’s post hoc test, p = 0.99). Ablated surface fish also demonstrated spike dynamics during swimming comparable to ablated and control cavefish (Pachón ablated, pre-swim: 18.6 ± 0.3 Hz; Pachón ablated, swimming: 14.7 ± 0.3 Hz). These findings indicate that efferents are necessary for inhibition of afferents during swimming in surface fish.

We compared lateral line activity between three different cave populations (Figure 5A); the Tinaja and Pachón populations, which are derived from similarly timed colonization events, and the Molino population that is derived from a more recent colonization event (Bradic et al., 2012; Dowling et al., 2002; Herman et al., 2018). Blind cavefish populations exhibited similar spontaneous spike rates across populations (F_2,17 = 0.68, p = 0.52), and swimming showed little effect on lateral line activity across blind cavefish populations (Figure 5B). We observed a minor decrease in afferent spike rates across cavefish populations and the relative change (i.e., inhibition) was similar in Pachón and Tinaja (Tukey’s post hoc test; Pachón: 0.28 ± 0.01; Tinaja: 0.32 ± 0.02; Figure 5C). Molino demonstrated an intermediate phenotype compared to Pachón and Tinaja (Tukey’s post hoc test; Molino: 0.23 ± 0.01; p < 0.01). The Molino population (new lineage) is most distantly related to the Pachón and Tinaja populations (old lineage), originating from a more recent surface fish colonization of caves thus providing phylogenetic evidence that coincides with statistically similar groupings (Herman et al., 2018). We examined the correlation between nonswimming and swimming spike rates across cave populations to determine whether the inhibitory effect was significant. Spike rates during swimming and pre-swim intervals were positively correlated in all cave populations, and afferent spike rates during swimming were not statistically distinguishable from unity across populations (Pachón: slope = 0.88, CI = −0.5 to 2.2; Tinaja: slope = 1.03, CI = −0.2 to 2.2; Molino: slope = 1.02, CI = 0.8 to 1.2; Figure 5D), indicating there was no significant decrease in afferent activity during swimming within blind cavefish populations.

Figure 5

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Our principal findings indicate elevated afferent spike activity and an increased responsiveness to hair cell deflection in cavefish. The increased afferent activity in cavefish is a likely consequence of eye loss, which has robust effects on other physiological systems (Duboué et al., 2011; Varatharasan et al., 2009). Heightened lateral line sensitivity in adults has been previously attributed to increased neuromast density in the ALL as well as increased hair cell quantities per neuromast (Jaggard et al., 2017; Lloyd et al., 2018; McHenry et al., 2008; Patton et al., 2010; Teyke, 1990; Yoffe et al., 2020; Yoffe et al., 2020; Yoshizawa et al., 2010). These differences do not exist in the posterior lateral line at the larval stage, allowing us a unique opportunity to investigate the neural mechanisms that can enhance flow sensing in a strong model for evolution. Our discovery of increased spontaneous activity that contributes to the enhanced evoked responses in cavefish is a powerful addition for flow sensing, and we predict that this in combination with the increased number of neuromasts in the ALL (Yoshizawa et al., 2010) is what ultimately enables cavefish to perform active-flow sensing.

Higher spontaneous activity is one of two mechanisms that are responsible for higher lateral line sensitivity. The other involves the inhibitory effects of the efferent system during swimming, a feedback mechanism that is conserved across the diversity of fishes (Flock and Russell, 1973; Lunsford et al., 2019; Montgomery et al., 1996; Montgomery and Bodznick, 1994; Roberts and Russell, 1972; Tricas and Highstein, 1991). This is true in swimming surface fish but not in cavefish. We found that three blind populations of cavefish (i.e., Pachón, Molino, and Tinaja) have repeatedly lost the capability for efferent modulation during swimming. When one considers that lateral line efferent activity can be driven by direct inputs from the visual system in zebrafish (Reinig et al., 2017), it seems possible that eye degeneration induces the loss of efferent function. This interpretation is consistent with the idea that lateral line efferents are thought to have undergone regressive loss before in the ancestral lamprey and hagfish (Kishida et al., 1987; Köppl, 2011; Koyama et al., 1990), both of which are nearly or completely blind during development (Dickson and Collard, 1979; Fernholm and Holmberg, 1975). However, our results illustrate that cholinergic efferent system is still present in cavefish, having lost functionality rather than disappearing (the efferent system is functional in surface fish). Exploring pre- and postsynaptic differences such as acetylcholine release or the density of nicotinic acetylcholine receptors (nAChR) may explain the reduced inhibitory efficacy and reveal molecular targets that could disrupt efferent function over the course of evolution (Dawkins et al., 2005).

Our demonstration of CD inactivity in cavefish provides an alternative mechanism by which evolution can enhance sensitivity, one that proceeds by decreasing inhibition rather than augmenting sensor morphology or density (Yamamoto et al., 2009; Yoshizawa et al., 2010; Yoshizawa et al., 2014). The impact of increasing sensitivity through a lack of inhibition is apparent during active-flow sensing in adult A. mexicanus. Active-flow sensing occurs during swimming and involves using the reflection of self-generated flow fields (Bleckmann et al., 1991) to follow walls (Patton et al., 2010), avoid obstacles (Teyke, 1985; Windsor et al., 2008), and discrimination between shapes (de Perera, 2004; Hassan, 1989; von Campenhausen et al., 1981). The repeated loss of inhibition across populations at the larval stage suggests that selection may act early in development on the efferent over afferent systems. Future experiments may test this hypothesis in adults, though it seems likely that this phenomenon would be preserved and only elaborated on throughout ontogeny, rather than reconfigured. Cavefish swim by using different body motions than surface fish. This finding has been interpreted as a mechanism to enhance wall following, which occurs when the bow wake of a swimming cavefish is reflected off of a solid surface and then detected (Patton et al., 2010; Sharma et al., 2009). Altered swimming kinematics are also thought to have arisen from a general increase in sensitivity to flow (Tan et al., 2011; Windsor et al., 2008). Our results provide an alternate suggestion; the lack of efferent function in cavefish precludes the sensory feedback necessary for sensing self-movement and body position in water (proprioception). CD, a parallel motor command that decreases the afferent activity of fishes when swimming, has recently been found to play a critical role in swimming efficiency by enabling the tracking of the traveling body wave during undulation (Skandalis et al., 2021). We hypothesize that the evolved loss of efferent function that enables cavefish to successfully avoid collisions in subterranean habitats is likely favored over optimizing swimming efficiency (Nakamura, 1997; Atasavun Uysal et al., 2010). We predict that loss of efferent function will be found in other blind hypogean species (Costa Sampaio et al., 2012) and that their respective surface populations will possess intact efferent functionality, as we have found in A. mexicanus. Neurophysiological recordings across a wider diversity of species would provide valuable insight into how efferent function may be sculpted by environmental selection and phylogenetic membership.

By employing neurophysiological approaches in the lateral line system of A. mexicanus for the first time, we show that elevated lateral line afferent activity and loss of efferent function have repeatedly evolved together across cavefish populations. Our findings come at a time when genetic tools in A. mexicanus enable brain-wide imaging and gene-editing based screening to identify candidate neural circuits and genes critical in the evolution of sensory systems (Jaggard et al., 2020; Warren et al., 2021). Going forward, applying genetic and electrophysiological tools in well-characterized neural circuits promises to inform our understanding of the evolution of neural systems and behavior more broadly.

Electrophysiology data generated and analyzed during this study are included as a supplementary file ('Supplementary File 1').

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Author details

1. Elias T Lunsford

   Department of Biology, University of Florida, Saint Augustine, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing - original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-3713-6994

2. Alexandra Paz

   Department of Biological Sciences, Florida Atlantic University, Jupiter, United States

   Contribution

   Formal analysis, Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

3. Alex C Keene

   Texas A&M University, College Station, United States

   Contribution

   Funding acquisition, Resources, Writing – review and editing

   Competing interests

   No competing interests declared

4. James C Liao

   Department of Biology, University of Florida, Saint Augustine, United States

   Contribution

   Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision, Validation, Writing – review and editing

   For correspondence

   jliao@whitney.ufl.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0181-6995

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