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Ehud Ahissar

Publications and source records attributed to Ehud Ahissar.

15 recordsLinked to original sources

Layer-specific touch-dependent facilitation and depression in the somatosensory cortex during active whisking.

Brains adapt to new situations by retuning their neurons. The most common form of neuronal adaptation, typically observed with repetitive stimulations of passive sensory organs, is depression (responses gradually decrease until stabilized). We studied cortical adaptation when stimuli are acquired by active movements of the sensory organ. In anesthetized rats, artificial whisking was induced at 5 Hz, and activity of individual neurons in layers 2-5 was recorded during whisking in air (Whisking condition) and whisking against an object (Touch condition). Response strengths were assessed by spike counts. Input-layer responses (layers 4 and 5a) usually facilitated during the whisking train, whereas superficial responses (layer 2/3) usually depressed. In layers 2/3 and 4, but not 5a, responses were usually stronger during touch trials than during whisking in air. Facilitations were specific to the protraction phase; during retraction, responses depressed in all layers and conditions. These dynamic processes were accompanied by a slow positive wave of activity progressing from superficial to deeper layers and lasting for approximately 1 s, during the transient phase of response. Our results indicate that, in the cortex, adaptation does not depend only on the level of activity or the frequency of its repetition but rather on the nature of the sensory information that is conveyed by that activity and on the processing layer. The input and laminar specificities observed here are consistent with the hypothesis that the paralemniscal layer 5a is involved in the processing of whisker motion, whereas the lemniscal barrels in layer 4 are involved in the processing of object identity.

Action Potentials↗

Haptic object localization in the vibrissal system: behavior and performance.

Using their large mystacial vibrissas, rats perform a variety of tasks, including localization and identification of objects. We report on the discriminatory thresholds and behavior of rats trained in a horizontal object localization task. Using an adaptive training procedure, rats learned to discriminate offsets in horizontal (anteroposterior) location with all, one row, or one arc of whiskers intact, but not when only a single whisker (C2) was intact on each cheek. However, rats initially trained with multiple whiskers typically improved when retested later with a single whisker intact. Individual rats reached localization thresholds as low as 0.24 mm (approximately 1 degree). Among the tested groups, localization acuity was finest (<1.5 mm) with rats that were initially trained with all whiskers and then trimmed to one arc of whiskers intact. Horizontal acuity was finer than the typical inter-vibrissal spacing (approximately 4.8 mm at contact points). Performance correlated with the net whisking spectral power in the range of 5-25 Hz but not in nonwhisking range of 30-50 Hz. Lesioning the facial motor nerves reduced performance to chance level. We conclude that horizontal object localization in the rat vibrissal system can reach hyperacuity level and is an active sensing process: whisker movements are both required and beneficiary, in a graded manner, for making accurate positional judgments.

Animals↗

Active sensation: insights from the rodent vibrissa sensorimotor system.

Rats sweep their vibrissae through space to locate objects in their immediate environment. In essence, their view of the proximal world is generated through pliable hairs that tap and palpate objects. The texture and shape of those objects must be discerned for the rat to assess the value of the object. Furthermore, the location of those objects must be specified with reference to the position of the rat's head for the rat to plan its movements. Recent in vivo and in vitro electrophysiological measurements provide insight into the algorithms and mechanisms that underlie these behavioral-based computations.

Action Potentials↗

Parallel thalamic pathways for whisking and touch signals in the rat.

In active sensation, sensory information is acquired via movements of sensory organs; rats move their whiskers repetitively to scan the environment, thus detecting, localizing, and identifying objects. Sensory information, in turn, affects future motor movements. How this motor-sensory-motor functional loop is implemented across anatomical loops of the whisker system is not yet known. While inducing artificial whisking in anesthetized rats, we recorded the activity of individual neurons from three thalamic nuclei of the whisker system, each belonging to a different major afferent pathway: paralemniscal, extralemniscal (a recently discovered pathway), or lemniscal. We found that different sensory signals related to active touch are conveyed separately via the thalamus by these three parallel afferent pathways. The paralemniscal pathway conveys sensor motion (whisking) signals, the extralemniscal conveys contact (touch) signals, and the lemniscal pathway conveys combined whisking-touch signals. This functional segregation of anatomical pathways raises the possibility that different sensory-motor processes, such as those related to motion control, object localization, and object identification, are implemented along different motor-sensory-motor loops.

Afferent Pathways↗

Temporal decoding by phase-locked loops: unique features of circuit-level implementations and their significance for vibrissal information processing.

Rhythmic active touch, such as whisking, evokes a periodic reference spike train along which the timing of a novel stimulus, induced, for example, when the whiskers hit an external object, can be interpreted. Previous work supports the hypothesis that the whisking-induced spike train entrains a neural implementation of a phase-locked loop (NPLL) in the vibrissal system. Here we extend this work and explore how the entrained NPLL decodes the delay of the novel, contact-induced stimulus and facilitates object localization. We consider two implementations of NPLLs, which are based on a single neuron or a neural circuit, respectively, and evaluate the resulting temporal decoding capabilities. Depending on the structure of the NPLL, it can lock in either a phase- or co-phase-sensitive mode, which is sensitive to the timing of the input with respect to the beginning of either the current or the next cycle, respectively. The co-phase-sensitive mode is shown to be unique to circuit-based NPLLs. Concentrating on temporal decoding in the vibrissal system of rats, we conclude that both the nature of the information processing task and the response characteristics suggest that the computation is sensitive to the co-phase. Consequently, we suggest that the underlying thalamocortical loop should implement a circuit-based NPLL.

Animals↗

Active construction of percepts about object location.

Mammals acquire much of their sensory information by actively moving their sensory organs. Rats, in particular, scan their surrounding environment with their whiskers. This form of active sensing induces specific patterns of temporal encoding of sensory information, which are based on a conversion of space into time via sensor movement. We investigate the ways in which object location is encoded by the whiskers and decoded by the brain. We recorded from first-order neurons located in the trigeminal ganglion (TG) of anaesthetized rats during epochs of artificial whisking induced by electrical stimulation of the facial motor nerve. We found that TG neurons encode the three positional coordinates with different codes. The horizontal coordinate (along the backward-forward axis) is encoded by two encoding schemes, both relying on the firing times of one type of TG neuron, the 'contact cell'. The radial coordinate (from face outward) is encoded primarily by the firing magnitude of another type of TG neurons, the 'pressure cell'. The vertical coordinate (from ground up) is encoded by the identity of activated neurons. The decoding schemes of at least some of these sensory cues, our data suggest, are also active: cortical representations are generated by a thalamic comparison of cortical expectations with incoming sensory data.

Animals↗

Coding of stimulus frequency by latency in thalamic networks through the interplay of GABAB-mediated feedback and stimulus shape.

A temporal sensory code occurs in posterior medial (POm) thalamus of the rat vibrissa system, where the latency for the spike rate to peak is observed to increase with increasing frequency of stimulation between 2 and 11 Hz. In contrast, the latency of the spike rate in the ventroposterior medial (VPm) thalamus is constant in this frequency range. We consider the hypothesis that two factors are essential for latency coding in the POm. The first is GABAB-mediated feedback inhibition from the reticular thalamic (Rt) nucleus, which provides delayed and prolonged input to thalamic structures. The second is sensory input that leads to an accelerating spike rate in brain stem nuclei. Essential aspects of the experimental observations are replicated by the analytical solution of a rate-based model with a minimal architecture that includes only the POm and Rt nuclei, i.e., an increase in stimulus frequency will increase the level of inhibitory output from Rt thalamus and lead to a longer latency in the activation of POm thalamus. This architecture, however, admits period-doubling at high levels of GABAB-mediated conductance. A full architecture that incorporates the VPm nucleus suppresses period-doubling. A clear match between the experimentally measured spike rates and the numerically calculated rates for the full model occurs when VPm thalamus receives stronger brain stem input and weaker GABAB-mediated inhibition than POm thalamus. Our analysis leads to the prediction that the latency code will disappear if GABAB-mediated transmission is blocked in POm thalamus or if the onset of sensory input is too abrupt. We suggest that GABAB-mediated inhibition is a substrate of temporal coding in normal brain function.

Action Potentials↗

Responses of trigeminal ganglion neurons to the radial distance of contact during active vibrissal touch.

Rats explore their environment by actively moving their whiskers. Recently, we described how object location in the horizontal (front-back) axis is encoded by first-order neurons in the trigeminal ganglion (TG) by spike timing. Here we show how TG neurons encode object location along the radial coordinate, i.e., from the snout outward. Using extracellular recordings from urethane-anesthetized rats and electrically induced whisking, we found that TG neurons encode radial distance primarily by the number of spikes fired. When an object was positioned closer to the whisker root, all touch-selective neurons recorded fired more spikes. Some of these cells responded exclusively to objects located near the base of whiskers, signaling proximal touch by an identity (labeled-line) code. A number of tonic touch-selective neurons also decreased delays from touch to the first spike and decreased interspike intervals for closer object positions. Information theory analysis revealed that near-certainty discrimination between two objects separated by 30% of the length of whiskers was possible for some single cells. However, encoding reliability was usually lower as a result of large trial-by-trial response variability. Our current findings, together with the identity coding suggested by anatomy for the vertical dimension and the temporal coding of the horizontal dimension, suggest that object location is encoded by separate neuronal variables along the three spatial dimensions: temporal for the horizontal, spatial for the vertical, and spike rate for the radial dimension.

Action Potentials↗

Tracking whisker and head movements in unrestrained behaving rodents.

Due to recent advances that enable real-time electrophysiological recordings in brains of awake behaving rodents, effective methods for analyzing the large amount of behavioral data thus generated, at millisecond resolution, are required. We describe a semiautomated, efficient method for accurate tracking of head and mystacial vibrissae (whisker) movements in freely moving rodents using high-speed video. By tracking the entire length of individual whiskers, we show how both location and shape of whiskers are relevant when describing the kinematics of whisker movements and whisker interactions with objects during a whisker-dependent task and exploratory behavior.

Animals↗

Neural signature of taste familiarity in the gustatory cortex of the freely behaving rat.

Ample data indicate that the gustatory cortex (GC) subserves the processing, encoding, and storage of taste information. To further elucidate the neural processes involved, we recorded multi-unit activity in the GC of the freely behaving rat as it became familiar with a novel tastant. Exposure to the tastant was performed over three 40- to 50-min sessions, 24 h apart. In each session, the tastant was presented repeatedly, 1 s at a time, with 10- to 12-s inter-trial intervals. The neural response to the tastant typically lasted 7 s. Our results show that the average neuronal response to the tastant increased as this tastant became familiar, but this increase was detected only during the last 5 s of the response. The increased response was not generalized to another tastant. Furthermore, our analysis suggests that specific neuronal populations subserve the processing of familiarity of specific tastants. The signature of familiarity was not detected in the course of the familiarization session, but only on the subsequent day, suggesting that its development involves slow post-acquisition processes. Our data are in line with the notion that GC neurons process multiple taste attributes, familiarity included, during different temporal phases of their response. The data also suggest that by default the brain considers a taste stimulus as novel, unless proven otherwise.

Animals↗

Encoding of vibrissal active touch.

Mammals acquire much of their sensory information by actively moving their sensory organs. Yet, the principles of encoding by active sensing are not known. Here we investigated the encoding principles of active touch by rat whiskers (vibrissae). We induced artificial whisking in anesthetized rats and recorded from first-order neurons in the trigeminal ganglion. During active touch, first-order trigeminal neurons presented a rich repertoire of responses, which could not be inferred from their responses to passive deflection stimuli. Individual neurons encoded four specific events: whisking, contact with object, pressure against object, and detachment from object. Whisking-responsive neurons fired at specific deflection angles, reporting the actual whiskers' position with high precision. Touch-responsive neurons encoded the horizontal coordinate of objects' position by spike timing. These findings suggest two specific encoding-decoding schemes for horizontal object position in the vibrissal system.

Action Potentials↗

Imaging spatiotemporal dynamics of surround inhibition in the barrels somatosensory cortex.

Sensory processing and its perception require that local information would also be available globally. Indeed, in the mammalian neocortex, local excitation spreads over large distances via the long-range horizontal connections in layer 2/3 and may spread over an entire cortical area if excitatory polysynaptic pathways are also activated. Therefore, a balance between local excitation and surround inhibition is required. Here we explore the spatiotemporal aspects of cortical depolarization and hyperpolarization of rats anesthetized with urethane. New voltage-sensitive dyes (VSDs) were used for high-resolution real-time visualization of the cortical responses to whisker deflections and cutaneous stimulations of the whisker pad. These advances facilitated imaging of ongoing activity and evoked responses even without signal averaging. We found that the motion of a single whisker evoked a cortical response exhibiting either one or three phases. During a triphasic response, there was first a cortical depolarization in a small cortical region the size of a single cortical barrel. Subsequently, this depolarization increased and spread laterally in an oval manner, preferentially along rows of the barrel field. During the second phase, the amplitude of the evoked response declined rapidly, presumably because of recurrent inhibition. Subsequently, the third phase exhibiting a depolarization rebound was observed and clear, and approximately 16 Hz oscillations were detected. Stimulus conditions revealing a net surround hyperpolarization during the second phase were also found. By using new, improved VSD, the present findings shed new light on the spatial parameters of the intricate spatiotemporal cortical interplay of inhibition and excitation.

Animals↗

Closed-loop neuronal computations: focus on vibrissa somatosensation in rat.

Two classes of neuronal architectures dominate in the ongoing debate on the nature of computing by nervous systems. The first is a predominantly feedforward architecture, in which local interactions among neurons within each processing stage play a less influential role compared with the drive of the input to that stage. The second class is a recurrent network architecture, in which the local interactions among neighboring neurons dominate the dynamics of neuronal activity so that the input acts only to bias or seed the state of the network. The study of sensorimotor networks, however, serves to highlight a third class of architectures, which is neither feedforward nor locally recurrent and where computations depend on large-scale feedback loops. Findings that have emerged from our laboratories and those of our colleagues suggest that the vibrissa sensorimotor system is involved in such closed-loop computations. In particular, single unit responses from vibrissa sensory and motor areas show generic signatures of phase-sensitive detection and control at the level of thalamocortical and corticocortical loops. These loops are likely to be components within a greater closed-loop vibrissa sensorimotor system, which optimizes sensory processing.

Afferent Pathways↗

Acetylcholine-dependent potentiation of temporal frequency representation in the barrel cortex does not depend on response magnitude during conditioning.

The response properties of neurons of the postero-medial barrel sub-field of the somatosensory cortex (the cortical structure receiving information from the mystacial vibrissae can be modified as a consequence of peripheral manipulations of the afferent activity. This plasticity depends on the integrity of the cortical cholinergic innervation, which originates at the nucleus basalis magnocellularis (NBM). The activity of the NBM is related to the behavioral state of the animal and the putative cholinergic neurons are activated by specific events, such as reward-related signals, during behavioral learning. Experimental studies on acetylcholine (ACh)-dependent cortical plasticity have shown that ACh is needed for both the induction and the expression of plastic modifications induced by sensory-cholinergic pairings. Here we review and discuss ACh-dependent plasticity and activity-dependent plasticity and ask whether these two mechanisms are linked. To address this question, we analyzed our data and tested whether changes mediated by ACh were activity-dependent. We show that ACh-dependent potentiation of response in the barrel cortex of rats observed after sensory-cholinergic pairing was not correlated to the changes in activity induced during pairing. Since these results suggest that the effect of ACh during pairing is not exerted through a direct control of the post-synaptic activity, we propose that ACh might induce its effect either pre- or post-synaptically through activation of second messenger cascades.

Acetylcholine↗