Sebastian Haidarliu

Transformation from temporal to rate coding in a somatosensory thalamocortical pathway.

The anatomical connections from the whiskers to the rodent somatosensory (barrel) cortex form two parallel (lemniscal and paralemniscal) pathways. It is unclear whether the paralemniscal pathway is directly involved in tactile processing, because paralemniscal neuronal responses show poor spatial resolution, labile latencies and strong dependence on cortical feedback. Here we show that the paralemniscal system can transform temporally encoded vibrissal information into a rate code. We recorded the representations of the frequency of whisker movement along the two pathways in anaesthetized rats. In response to varying stimulus frequencies, the lemniscal neurons exhibited amplitude modulations and constant latencies. In contrast, paralemniscal neurons in both thalamus and cortex coded the input frequency as changes in latency. Because the onset latencies increased and the offset latencies remained constant, the latency increments were translated into a rate code: increasing onset latencies led to lower spike counts. A thalamocortical loop that includes cortical oscillations and thalamic gating can account for these results. Thus, variable latencies and effective cortical feedback in the paralemniscal system can serve the processing of temporal sensory cues, such as those that encode object location during whisking. In contrast, fixed time locking in the lemniscal system is crucial for reliable spatial processing.

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.

A neuronal analogue of state-dependent learning

State-dependent learning is a phenomenon in which the retrieval of newly acquired information is possible only if the subject is in the same sensory context and physiological state as during the encoding phase. In spite of extensive behavioural and pharmacological characterization, no cellular counterpart of this phenomenon has been reported. Here we describe a neuronal analogue of state-dependent learning in which cortical neurons show an acetylcholine-dependent expression of an acetylcholine-induced functional plasticity. This was demonstrated on neurons of rat somatosensory ‘barrel’ cortex, whose tunings to the temporal frequency of whisker deflections were modified by cellular conditioning. Pairing whisker stimulation with acetylcholine applied iontophoretically yielded selective lasting modification of responses, the expression of which depended on the presence of exogenous acetylcholine. Administration of acetylcholine during testing revealed frequency-specific changes in response that were not expressed when tested without acetylcholine or when the muscarinic antagonist, atropine, was applied concomitantly. Our results suggest that both acquisition and recall can be controlled by the cortical release of acetylcholine.

Size gradients of barreloids in the rat thalamus.

The spatial organization of the anatomical structures along the trigeminal afferent pathway of the rat conserves the topographical order of the receptor sheath: The brainstem barrelettes, thalamic barreloids, and cortical barrels all reflect the arrangement of whiskers across the mystacial pad. Although both the amount of innervation in the mystacial pad and the size of cortical barrels were shown previously to exhibit increasing gradients toward the ventral and caudal whiskers, whether similar gradients existed in the brainstem and thalamus was not known. Here, the authors investigated the size gradients of the barreloids in the ventral posteromedial nucleus of the rat thalamus. Because the angles used to cut the brain were crucial to this study, the optimal cutting angles were determined first for visualization of individual barreloids and of the entire barreloid field. Individual barreloids, arcs, and rows as well as entire barreloid fields were clearly visualized using cytochrome oxidase staining of brain slices that were cut with the optimal cutting angles. For the first five arcs (including straddlers), the length of barreloids increased in the direction of dorsal‐to‐ventral whiskers and of caudal‐to‐rostral whiskers. These gradients reveal an inverse relationship between the size of barreloids and whiskers (length and follicle diameter) along arcs and rows. The largest barreloids in the ventral posteromedial nucleus were those that represent whiskers C2–C4, D2–D4, and E2–E4, which are neither the largest nor the most innervated whiskers in the mystacial pad. This implies that the extended representation is not merely a reflection of peripheral innervation biases and probably serves an as yet unknown processing function. J. Comp. Neurol. 429:372–387, 2001.

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 ∼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.

Muscle Architecture in the Mystacial Pad of the Rat

The vibrissal system of the rat is an example of active tactile sensing, and has recently been used as a prototype in construction of touch‐oriented robots. Active vibrissal exploration and touch are enabled and controlled by musculature of the mystacial pad. So far, knowledge about motor control of the rat vibrissal system has been extracted from what is known about the vibrissal systems of other species, mainly mice and hamsters, since a detailed description of the musculature of the rat mystacial pad was lacking. In the present work, the musculature of the rat mystacial pad was revealed by slicing the mystacial pad in four different planes, staining of mystacial pad slices for cytochrome oxidase, and tracking spatial organization of mystacial pad muscles in consecutive slices. We found that the rat mystacial pad contains four superficial extrinsic muscles and five parts of the M. nasolabialis profundus. The connection scheme of the three parts of the M. nasolabialis profundus is described here for the first time. These muscles are inserted into the plate of the mystacial pad, and thus, their contraction causes whisker retraction. All the muscles of the rat mystacial pad contained three types of skeletal striated fibers (red, white, and intermediate). Although the entire rat mystacial pad usually functions as unity, our data revealed its structural segmentation into nasal and maxillary subdivisions. The mechanisms of whisking in the rat, and hypotheses concerning biomechanical interactions during whisking, are discussed with respect to the muscle architecture of the rat mystacial pad. Anat Rec 293:1192–1206, 2010.

A multi-electrode array for combined microiontophoresis and multiple single-unit recordings.

A remotely controlled multi-electrode array, equipped with a combined electrode (CE) and 3 regular tungsten-in-glass electrodes (TEs) is described. The CE enables ejection of different neuroactive substances from 6 barrels and recording of single-unit activity from the etched tungsten rod placed in the central glass capillary. The CE is prepared with standard tungsten rod, glass-capillaries, and regular micropipette pullers. Such CEs possess a good stiffness-flexibility balance, length, easy cell isolation, high stability of recordings, effective ejection properties, and ability to survive penetration of dura. The efficiency of a 4-electrode array, including the CE, was tested by recording the effects of extracellularly ejected drugs (glutamate, acetylcholine and atropine) on single neurons in the auditory cortex of anesthetized guinea pigs. Induced modifications of single-neuron firing patterns and evoked responses were in agreement with the known effects of individual and combined applications of these drugs. Using this multi-electrode array and spike sorting techniques, the pharmacological environment of up to 12 simultaneously recorded cells can be modulated, and its effect on single neurons and on their interactions can be monitored at distances of up to 900 microns from the CEs tip.

Possible involvement of neuromodulatory systems in cortical Hebbian-like plasticity

Plasticity of neuronal covariances (functional plasticity) is controlled by behavior (Ahissar et al (1992) Science 257, 1412-1415). Whether this behavioral control involves neuromodulatory systems was tested by examining the effect of acetylcholine (ACh) and noradrenaline (NE) on functional plasticity in anesthetized animals and by comparing the effects of these neuromodulators in an anesthetized preparation to that of behavior in awake animals. Local ionotophoretic applications of these drugs during manipulations of activity covariance in guinea pig auditory cortex did not mimic the behavioral control of functional plasticity that was previously observed in awake monkeys. Thus, the hypotheses according to which these neuromodulators control functional plasticity independent of their concentration and time of release were not supported by our data. The significant plasticity induced nevertheless, by some of the conditionings in the presence of ACh and NE, suggests that factors, other than those that were experimentally controlled, could regulate this plasticity. These factors could be among others the timing of drug(s) applications relative to the conditioning time, the local concentrations of the drug(s) and/or the site of application with respect to the relevant synapses.

Spatial organization of facial vibrissae and cortical barrels in the guinea pig and golden hamster

The arrangements of vibrissae in guinea pigs and golden hamsters were previously reported to be different from those in mice and rats. Whereas the mystacial pads in mice and rats include four straddlers and five rows of vibrissae, guinea pigs were described to possess six rows of irregularly aligned mystacial vibrissae and no straddlers, and golden hamsters to include seven vibrissal rows and also no straddlers. We found that all of these four species possess similar vibrissal arrangements within the mystacial pad. To demonstrate this similarity, we developed a new method of sinus hair visualization in flattened and cleared preparations of the mystacial pad. Intrinsic muscles of the mystacial pad that were revealed in thick histological preparations showed clearly the structural and functional relationships between straddlers and vibrissal rows. To verify this finding, and to extend the knowledge of vibrissal cortical representations in guinea pigs and golden hamsters, we have investigated the spatial organization and the functional vibrissal representations of barrels in the posteromedial barrel subfield (PMBSF) of these rodents. The barrel morphology was clearly preserved in Nissl‐stained sections and sections processed for cytochrome oxidase of flattened cerebral cortices. We demonstrate that the vibrissal arrangement in the mystacial pad is replicated in the PMBSF of guinea pigs and golden hamsters and that this arrangement is similar to that found in mice and rats. To facilitate comparative studies, these findings strongly recommend the use, in guinea pigs and golden hamsters, of the same classifications and nomenclatures that are used in mice and rats to describe mystacial vibrissae and cortical barrels. J. Comp. Neurol. 385:515–527, 1997.

Dorsorostral snout muscles in the rat subserve coordinated movement for whisking and sniffing.

Histochemical examination of the dorsorostral quadrant of the rat snout revealed superficial and deep muscles that are involved in whisking, sniffing, and airflow control. The part of M. nasolabialis profundus that acts as an intrinsic (follicular) muscle to facilitate protraction and translation of the vibrissae is described. An intraturbinate and selected rostral‐most nasal muscles that can influence major routs of inspiratory airflow and rhinarial touch through their control of nostril configuration, atrioturbinate and rhinarium position, were revealed. Anat Rec, 2012.