scholarly journals Sensory computations in the cuneate nucleus of macaques

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.

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.


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.


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 11 (1) ◽  
Author(s):  
Jermyn Z. See ◽  
Natsumi Y. Homma ◽  
Craig A. Atencio ◽  
Vikaas S. Sohal ◽  
Christoph E. Schreiner

AbstractNeuronal activity in auditory cortex is often highly synchronous between neighboring neurons. Such coordinated activity is thought to be crucial for information processing. We determined the functional properties of coordinated neuronal ensembles (cNEs) within primary auditory cortical (AI) columns relative to the contributing neurons. Nearly half of AI cNEs showed robust spectro-temporal receptive fields whereas the remaining cNEs showed little or no acoustic feature selectivity. cNEs can therefore capture either specific, time-locked information of spectro-temporal stimulus features or reflect stimulus-unspecific, less-time specific processing aspects. By contrast, we show that individual neurons can represent both of those aspects through membership in multiple cNEs with either high or absent feature selectivity. These associations produce functionally heterogeneous spikes identifiable by instantaneous association with different cNEs. This demonstrates that single neuron spike trains can sequentially convey multiple aspects that contribute to cortical processing, including stimulus-specific and unspecific information.


1992 ◽  
Vol 68 (2) ◽  
pp. 518-527 ◽  
Author(s):  
T. P. Pons ◽  
P. E. Garraghty ◽  
M. Mishkin

1. Selective ablations of the hand representations in postcentral cortical areas 3a, 3b, 1, and 2 were made in different combinations to determine each area's contribution to the responsivity and modality properties of neurons in the hand representation in SII. 2. Ablations that left intact only the postcentral areas that process predominantly cutaneous inputs (i.e., areas 3b and 1) yielded SII recording sites responsive to cutaneous stimulation and none driven exclusively by high-intensity or "deep" stimulation. Conversely, ablations that left intact only the postcentral areas that process predominantly deep receptor inputs (i.e., areas 3a and 2) yielded mostly SII recording sites that responded exclusively to deep stimulation. 3. Ablations that left intact only area 3a or only area 2 yielded substantial and roughly equal reductions in the number of deep receptive fields in SII. By contrast, ablations that left intact only area 3b or only area 1 yielded unequal reductions in the number of cutaneous receptive fields in SII: a small reduction when area 3b alone was intact but a somewhat larger one when only area 1 was intact. 4. Finally, when the hand representation in area 3b was ablated, leaving areas 3a, 1, and 2 fully intact, there was again a substantial reduction in the encounter rate of cutaneous receptive fields. 5. The partial ablations often led to unresponsive sites in the SII hand representation. In SII representations other than of the hand no such unresponsive sites were found and there were no substantial changes in the ratio of cutaneous to deep receptive fields, indicating that the foregoing results were not due to long-lasting postsurgical depression or effects of anesthesia. 6. The findings indicate that modality-specific information is relayed from postcentral cortical areas to SII along parallel channels, with cutaneous inputs transmitted via areas 3b and 1, and deep inputs via areas 3a and 2. Further, area 3b provides the major source of cutaneous input to SII, directly and perhaps also via area 1. 7. The results are in line with accumulating anatomic and electrophysiologic evidence pointing to an evolutionary shift in the organization of the somatosensory system from the general mammalian plan, in which tactile information is processed in parallel in SI and SII, to a new organization in higher primates in which the processing of tactile information proceeds serially from SI to SII. The presumed functional advantages of this evolutionary shift are unknown.


1998 ◽  
Vol 80 (6) ◽  
pp. 2882-2892 ◽  
Author(s):  
Christopher I. Moore ◽  
Sacha B. Nelson

Moore, Christopher I. and Sacha B. Nelson. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80: 2882–2892, 1998. Whole cell recordings of synaptic responses evoked by deflection of individual vibrissa were obtained from neurons within adult rat primary somatosensory cortex. To define the spatial and temporal properties of subthreshold receptive fields, the spread, amplitude, latency to onset, rise time to half peak amplitude, and the balance of excitation and inhibition of subthreshold input were quantified. The convergence of information onto single neurons was found to be extensive: inputs were consistently evoked by vibrissa one- and two-away from the vibrissa that evoked the largest response (the “primary vibrissa”). Latency to onset, rise time, and the incidence and strength of inhibitory postsynaptic potentials (IPSPs) varied as a function of position within the receptive field and the strength of evoked excitatory input. Nonprimary vibrissae evoked smaller amplitude subthreshold responses [primary vibrissa, 9.1 ± 0.84 (SE) mV, n = 14; 1-away, 5.1 ± 0.5 mV, n = 38; 2-away, 3.7 ± 0.59 mV, n = 22; 3-away, 1.3 ± 0.70 mV, n = 8] with longer latencies (primary vibrissa, 10.8 ± 0.80 ms; 1-away, 15.0 ± 1.2 ms; 2-away, 15.7 ± 2.0 ms). Rise times were significantly faster for inputs that could evoke action potential responses (suprathreshold, 4.1 ± 1.3 ms, n = 8; subthreshold, 12.4 ± 1.5 ms, n = 61). In a subset of cells, sensory evoked IPSPs were examined by deflecting vibrissa during injection of hyperpolarizing and depolarizing current. The strongest IPSPs were evoked by the primary vibrissa ( n = 5/5), but smaller IPSPs also were evoked by nonprimary vibrissae ( n = 8/13). Inhibition peaked by 10–20 ms after the onset of the fastest excitatory input to the cortex. This pattern of inhibitory activity led to a functional reversal of the center of the receptive field and to suppression of later-arriving and slower-rising nonprimary inputs. Together, these data demonstrate that subthreshold receptive fields are on average large, and the spatio-temporal dynamics of these receptive fields vary as a function of position within the receptive field and strength of excitatory input. These findings constrain models of suprathreshold receptive field generation, multivibrissa interactions, and cortical plasticity.


1995 ◽  
Vol 200 (1) ◽  
pp. 25-28 ◽  
Author(s):  
Alfons Schnitzler ◽  
Riitta Salmelin ◽  
Stephan Salenius ◽  
Veikko Jousmäki ◽  
Riitta Hari

2017 ◽  
Vol 284 (1862) ◽  
pp. 20170969 ◽  
Author(s):  
Brandon Pratt ◽  
Tanvi Deora ◽  
Thomas Mohren ◽  
Thomas Daniel

Flying insects use feedback from various sensory modalities including vision and mechanosensation to navigate through their environment. The rapid speed of mechanosensory information acquisition and processing compensates for the slower processing times associated with vision, particularly under low light conditions. While halteres in dipteran species are well known to provide such information for flight control, less is understood about the mechanosensory roles of their evolutionary antecedent, wings. The features that wing mechanosensory neurons (campaniform sensilla) encode remains relatively unexplored. We hypothesized that the wing campaniform sensilla of the hawkmoth, Manduca sexta, rapidly and selectively extract mechanical stimulus features in a manner similar to halteres. We used electrophysiological and computational techniques to characterize the encoding properties of wing campaniform sensilla. To accomplish this, we developed a novel technique for localizing receptive fields using a focused IR laser that elicits changes in the neural activity of mechanoreceptors. We found that (i) most wing mechanosensors encoded mechanical stimulus features rapidly and precisely, (ii) they are selective for specific stimulus features, and (iii) there is diversity in the encoding properties of wing campaniform sensilla. We found that the encoding properties of wing campaniform sensilla are similar to those for haltere neurons. Therefore, it appears that the neural architecture that underlies the haltere sensory function is present in wings, which lends credence to the notion that wings themselves may serve a similar sensory function. Thus, wings may not only function as the primary actuator of the organism but also as sensors of the inertial dynamics of the animal.


2005 ◽  
Vol 16 (6) ◽  
pp. 791-810 ◽  
Author(s):  
Banu Tutunculer ◽  
Guglielmo Foffani ◽  
B. Timothy Himes ◽  
Karen A. Moxon

1999 ◽  
Vol 81 (2) ◽  
pp. 825-834 ◽  
Author(s):  
Iran Salimi ◽  
Thomas Brochier ◽  
Allan M. Smith

Neuronal activity in somatosensory cortex of monkeys using a precision grip. I. Receptive fields and discharge patterns. Three adolescent Macaca fascicularis monkeys weighing between 3.5 and 4 kg were trained to use a precision grip to grasp a metal tab mounted on a low friction vertical track and to lift and hold it in a 12- to 25-mm position window for 1 s. The surface texture of the metal tab in contact with the fingers and the weight of the object could be varied. The activity of 386 single cells with cutaneous receptive fields contacting the metal tab were recorded in Brodmann’s areas 3b, 1, 2, 5, and 7 of the somatosensory cortex. In this first of a series of papers, we describe three types of discharge pattern, the receptive-field properties, and the anatomic distribution of the neurons. The majority of the receptive fields were cutaneous and covered less than one digit, and a χ2 test did not reveal any significant differences in the Brodmann’s areas representing the thumb and index finger. Two broad categories of discharge pattern cells were identified. The first category, dynamic cells, showed a brief increase in activity beginning near grip onset, which quickly subsided despite continued pressure applied to the receptive field. Some of the dynamic neurons responded to both skin indentation and release. The second category, static cells, had higher activity during the stationary holding phase of the task. These static neurons demonstrated varying degrees of sensitivity to rates of pressure change on the skin. The percentage of dynamic versus static cells was about equal for areas 3b, 2, 5, and 7. Only area 1 had a higher proportion of dynamic cells (76%). A third category was identified that contained cells with significant pregrip activity and included cortical cells with both dynamic or static discharge patterns. Cells in this category showed activity increases before movement in the absence of receptive-field stimulation, suggesting that, in addition to peripheral cutaneous input, these cells also receive strong excitation from movement-related regions of the brain.


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