scholarly journals Modulation of cutaneous responses in the cuneate nucleus of macaques during active movement

2021 ◽  
Author(s):  
Qinpu He ◽  
Christopher S Versteeg ◽  
Aneesha K Suresh ◽  
Lee E Miller ◽  
Sliman J Bensmaia

To achieve stable and precise movement execution, the sensorimotor system integrates exafferent sensory signals originating from interactions with the external world and reafferent signals caused by our own movements. This barrage of sensory information is regulated such that behaviorally relevant signals are boosted at the expense of irrelevant ones. For example, sensitivity to touch is reduced during movement - when cutaneous signals caused by skin stretch are expected and uninteresting - a phenomenon reflected in a decreased cutaneous responsiveness in thalamus and cortex. Some evidence suggests that movement gating of touch may originate from the cuneate nucleus (CN), the first recipient of signals from tactile nerve fibers along the dorsal columns medial lemniscal pathway. To test this possibility, we intermittently delivered mechanical pulses to the receptive fields (RFs) of identified cutaneous CN neurons as monkeys performed a reach-to-grasp task. As predicted, we found that the cutaneous responses of individual CN neurons were reduced during movement. However, this movement gating of cutaneous signals was observed for CN neurons with RFs on the arm but not those with RFs on the hand. We conclude that sensory gating occurs in the first processing stage along the somatosensory neuraxis and sculpts incoming signals according to their task relevance.

2021 ◽  
Vol 118 (49) ◽  
pp. e2115772118
Author(s):  
Aneesha K. Suresh ◽  
Charles M. Greenspon ◽  
Qinpu He ◽  
Joshua M. Rosenow ◽  
Lee E. Miller ◽  
...  

Tactile nerve fibers fall into a few classes that can be readily distinguished based on their spatiotemporal response properties. Because nerve fibers reflect local skin deformations, they individually carry ambiguous signals about object features. In contrast, cortical neurons exhibit heterogeneous response properties that reflect computations applied to convergent input from multiple classes of afferents, which confer to them a selectivity for behaviorally relevant features of objects. The conventional view is that these complex response properties arise within the cortex itself, implying that sensory signals are not processed to any significant extent in the two intervening structures—the cuneate nucleus (CN) and the thalamus. To test this hypothesis, we recorded the responses evoked in the CN to a battery of stimuli that have been extensively used to characterize tactile coding in both the periphery and cortex, including skin indentations, vibrations, random dot patterns, and scanned edges. We found that CN responses are more similar to their cortical counterparts than they are to their inputs: CN neurons receive input from multiple classes of nerve fibers, they have spatially complex receptive fields, and they exhibit selectivity for object features. Contrary to consensus, then, the CN plays a key role in processing tactile information.


2021 ◽  
Author(s):  
Aneesha K Suresh ◽  
Charles M. Greenspon ◽  
Qinpu He ◽  
Joshua M Rosenow ◽  
Lee E Miller ◽  
...  

In primates, the responses of individual neurons in primary somatosensory cortex (S1) reflect convergent input from multiple classes of nerve fibers and are selective for behaviorally relevant stimulus features. The conventional view is that these response properties reflect computations that are effected in cortex, implying that sensory signals are not meaningfully processed in the two intervening structures - the Cuneate Nucleus (CN) and the thalamus. To test this hypothesis, we recorded the responses evoked in CN to a battery of stimuli that have been extensively used to characterize tactile coding, including skin indentations, vibrations, random dot patterns, and scanned edges. We found that CN responses are more similar to their S1 counterparts than they are to their inputs: CN neurons receive input from multiple sub-modalities, have spatially complex receptive fields, and exhibit selectivity for geometric features. Thus, CN plays a key role in the processing of tactile information.


2008 ◽  
Vol 99 (2) ◽  
pp. 866-875 ◽  
Author(s):  
Richard D. Lane ◽  
Charles P. Pluto ◽  
Cynthia L. Kenmuir ◽  
Nicolas L. Chiaia ◽  
Richard D. Mooney

Neonatal forelimb amputation in rats produces sprouting of sciatic nerve afferent fibers into the cuneate nucleus (CN) and results in 40% of individual CN neurons expressing both forelimb-stump and hindlimb receptive fields. The forelimb-stump region of primary somatosensory cortex (S-I) of these rats contains neurons in layer IV that express both stump and hindlimb receptive fields. However, the source of the aberrant input is the S-I hindlimb region conveyed to the S-I forelimb-stump region via intracortical projections. Although the reorganization in S-I reflects changes in cortical circuitry, it is possible that these in turn are dependent on the CN reorganization. The present study was designed to directly test whether the sprouting of sciatic afferents into the CN is required for expression of the hindlimb inputs in the S-I forelimb-stump field. To inhibit sprouting, neurotrophin-3 (NT-3) was applied to the cut nerves following amputation. At P60 or older, NT-3-treated rats showed minimal sciatic nerve fibers in the CN. Multiunit electrophysiological recordings in the CN of NT-3-treated, amputated rats revealed 6.3% of sites were both stump/hindlimb responsive, compared with 30.5% in saline-treated amputated animals. Evaluation of the S-I following GABA receptor blockade, revealed that the percentage of hindlimb responsive sites in the stump representation of the NT-3-treated rats (34.2%) was not significantly different from that in saline-treated rats (31.5%). These results indicate that brain stem reorganization in the form of sprouting of sciatic afferents into the CN is not necessary for development of anomalous hindlimb receptive fields within the S-I forelimb/stump region.


Segmental sensory receptive fields in axolotl hindlimb skin were mapped during extracellular recording of nerve responses to light tactile stimulation. Normally, cutaneous sensory innervation patterns for a given pair of left and right hindlimbs were similar, but there was variability among animals. Individual cutaneous fibres innervated a solitary receptive field whose borders were sharply defined. When spinal nerves were crushed or cut and allowed to regrow the receptive fields re-established were similar to those on the normal contralateral limb. However, many single cutaneous fibres innervated multiple receptive fields. After cutting and interchanging the two major limb nerve branches, regenerating cutaneous nerves tended to innervate skin toward which they were directed, and receptive fields did not resemble the patterns on the control limb skin. This contrasts with the results following the same operations on the motor innervation where patterns of re-innervation do resemble the control. Regenerating cutaneous fibres apparently cannot relocate their respective original cutaneous addresses, but readily re-innervate foreign skin areas. Nerves regenerating after a crush or cut appear to follow mechanical and/or biochemical orienting clues within the nerve trunks for restoration of typical innervation patterns. It is not known how the axolotl central nervous system copes with cutaneous sensory information from mislocated nerve terminals.


1984 ◽  
Vol 52 (6) ◽  
pp. 1200-1212 ◽  
Author(s):  
M. E. McCourt ◽  
G. H. Jacobs

Directional units in the optic nerve of the California ground squirrel (Spermophilus beecheyi) were studied with respect to their response to diffuse light, preferred directions of motion, tuning for preferred direction, the relationship between spatial and directional tuning characteristics, and receptive-field size and areal summating properties. Directional units in the ground squirrel optic nerve are of the “on-off” type. No purely on or off units were encountered in a sample of 356 directionally selective fibers. The distribution of preferred directions of image motion for 356 units was significantly anisotropic; greater than 50% of the directional units prefer motion in the direction of the superior-nasal visual quadrant. Mean directional bandwidth, measured at half-amplitude response, for 39 units was 88.5 degrees. The distribution of directional bandwidths suggests that two subpopulations of directional units may exist a broadly tuned (106.4 degrees bandwidth) group preferring image motion in the superior-nasal direction, and a narrowly tuned group (59.9 degrees bandwidth) with a uniform distribution of preferred direction. Tuning for direction of motion and for spatial frequency were significantly positively correlated in a sample of 35 directional units. Area-vs.-response measures for directional units show that they possess excitatory discharge centers with a concentric antagonistic surround, plus a larger suppressive surround activated specifically by moving luminance contours, which may be asymmetric. Critical activation areas for directional units, as measured along orthogonal orientations, were highly positively correlated. This suggests that these receptive fields possess the property of linear spatial summation, not of luminance flux, but of areas of moving luminance contours.


1987 ◽  
Vol 57 (4) ◽  
pp. 938-961 ◽  
Author(s):  
D. J. Surmeier ◽  
A. L. Towe

Fifty-two slowly adapting proprioceptive neurons in the cuneate nucleus of chloralose-anesthetized cats were studied. Recordings were made from 3 mm rostral to the obex to 5 mm caudal. The highest densities of proprioceptive neurons were found above and more than 3 mm caudal to the obex. Analysis of the spike trains produced with the forelimb held fixed revealed three basic periodic patterns. Neurons exhibiting these patterns were partitioned into three groups, referred to as the A, B, and C classes. Class A neurons (42%; 22/52) produced regular spike trains that were qualitatively similar to muscle spindle fibers. Interval distributions for this class were typically unimodal and slightly positively skewed. Adjacent intervals were frequently positively correlated. Spectral analysis suggested that 91% of class A spike trains had one to two periodic components. Class B neurons (21%; 11/52) had additional spikes interposed in their periodic discharge; these "interrupting" spikes did not significantly alter the timing of the dominant periodic discharge. Interval distributions were typically bimodal and adjacent intervals were negatively correlated. Spectral analysis suggested that two or more periodic components were present in their spike trains. Class C neurons (36%; 26/52) had spike trains with a basic rhymicity, but when this specific discharge was interrupted, the subsequent interval was near modal length; thus, they were "reset." Interval distributions were usually multimodal and adjacent intervals were frequently negatively correlated. Spectral analysis suggested that C spike trains usually had four or more periodic components. Estimates of information-carrying capacity of each class using a mean rate code and those of primary muscle spindle fibers suggested that a sizable information loss may occur in synaptic transmission. This potential loss was smaller for A-neurons (40%) than for B- (69%) or C-neurons (64%). Electrical stimulation of cutaneous structures influenced 55% (22/52) of the sample. All were members of the B and C classes. Responses were typically biphasic. The cutaneous receptive fields nearly always included a portion of the forepaw. No relationship was found between movement sensitivity and receptive field topography. Contralateral input was found in half (10/20) the neurons tested.


2010 ◽  
Vol 104 (2) ◽  
pp. 675-684 ◽  
Author(s):  
Yen-Chyi Liu ◽  
Jens Herberholz

Crayfish ( Procambarus clarkii ) have bilateral pairs of giant interneurons that control rapid escape movements in response to predatory threats. The medial giant neurons (MGs) can be made to fire an action potential by visual or tactile stimuli directed to the front of the animal and this leads to an escape tail-flip that thrusts the animal directly backward. The lateral giant neurons (LGs) can be made to fire an action potential by strong tactile stimuli directed to the rear of the animal, and this produces flexions of the abdomen that propel the crayfish upward and forward. These observations have led to the notion that the receptive fields of the giant neurons are locally restricted and do not overlap with each other. Using extra- and intracellular electrophysiology in whole animal preparations of juvenile crayfish, we found that the receptive fields of the LGs are far more extensive than previously assumed. The LGs receive excitatory inputs from descending interneurons originating in the brain; these interneurons can be activated by stimulation of the antenna II nerve or the protocerebral tract. In our experiments, descending inputs alone could not cause action potentials in the LGs, but when paired with excitatory postsynaptic potentials elicited by stimulation of tail afferents, the inputs summed to yield firing. Thus the LG escape neurons integrate sensory information received through both rostral and caudal receptive fields, and excitatory inputs that are activated rostrally can bring the LGs' membrane potential closer to threshold. This enhances the animal's sensitivity to an approaching predator, a finding that may generalize to other species with similarly organized escape systems.


2015 ◽  
Vol 113 (5) ◽  
pp. 1545-1555 ◽  
Author(s):  
Douglas A. Ruff ◽  
Richard T. Born

Attending to a stimulus modulates the responses of sensory neurons that represent features of that stimulus, a phenomenon named “feature attention.” For example, attending to a stimulus containing upward motion enhances the responses of upward-preferring direction-selective neurons in the middle temporal area (MT) and suppresses the responses of downward-preferring neurons, even when the attended stimulus is outside of the spatial receptive fields of the recorded neurons (Treue S, Martinez-Trujillo JC. Nature 399: 575–579, 1999). This modulation renders the representation of sensory information across a neuronal population more selective for the features present in the attended stimulus (Martinez-Trujillo JC, Treue S. Curr Biol 14: 744–751, 2004). We hypothesized that if feature attention modulates neurons according to their tuning preferences, it should also be sensitive to their tuning strength, which is the magnitude of the difference in responses to preferred and null stimuli. We measured how the effects of feature attention on MT neurons in rhesus monkeys ( Macaca mulatta) depended on the relationship between features—in our case, direction of motion and binocular disparity—of the attended stimulus and a neuron's tuning for those features. We found that, as for direction, attention to stimuli containing binocular disparity cues modulated the responses of MT neurons and that the magnitude of the modulation depended on both a neuron's tuning preferences and its tuning strength. Our results suggest that modulation by feature attention may depend not just on which features a neuron represents but also on how well the neuron represents those features.


2017 ◽  
Vol 118 (2) ◽  
pp. 1210-1220 ◽  
Author(s):  
Elzbieta Jankowska ◽  
Dominik Kaczmarek ◽  
Francesco Bolzoni ◽  
Ingela Hammar

The study indicates a new form of plasticity of myelinated fibers. The differences in time course of DC-evoked increases in the excitability of myelinated nerve fibers in the dorsal columns and in preterminal axonal branches suggest that distinct mechanisms are involved in them. The results show that combining epidural stimulation and transspinal DC polarization may dramatically improve their outcome and result in more effective pain control and the return of impaired motor functions.


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