Spatial structure of multiwhisker receptive fields in the barrel cortex is stimulus dependent

2011 ◽  
Vol 106 (2) ◽  
pp. 986-998 ◽  
Author(s):  
Julie Le Cam ◽  
Luc Estebanez ◽  
Vincent Jacob ◽  
Daniel E. Shulz

The tactile sensations mediated by the whisker-trigeminal system allow rodents to efficiently detect and discriminate objects. These capabilities rely strongly on the temporal and spatial structure of whisker deflections. Subthreshold but also spiking receptive fields in the barrel cortex encompass a large number of vibrissae, and it seems likely that the functional properties of these multiwhisker receptive fields reflect the multiple-whisker interactions encountered by the animal during exploration of its environment. The aim of this study was to examine the dependence of the spatial structure of cortical receptive fields on stimulus parameters. Using a newly developed 24-whisker stimulation matrix, we applied a forward correlation analysis of spiking activity to randomized whisker deflections (sparse noise) to characterize the receptive fields that result from caudal and rostral directions of whisker deflection. We observed that the functionally determined principal whisker, the whisker eliciting the strongest response with the shortest latency, differed according to the direction of whisker deflection. Thus, for a given neuron, maximal responses to opposite directions of whisker deflections could be spatially separated. This spatial separation resulted in a displacement of the center of mass between the rostral and caudal subfields and was accompanied by differences between response latencies in rostral and caudal directions of whisker deflection. Such direction-dependent receptive field organization was observed in every cortical layer. We conclude that the spatial structure of receptive fields in the barrel cortex is not an intrinsic property of the neuron but depends on the properties of sensory input.

2010 ◽  
Vol 103 (2) ◽  
pp. 709-724 ◽  
Author(s):  
Nicholas Wright ◽  
Kevin Fox

Layer IV of the barrel cortex contains an anatomical map of the contralateral whisker pad, which serves as a useful reference in relating receptive field properties of cells to the cortical columns in which they reside. Recent studies have shown that the degree to which the surround receptive fields of layer IV cells are generated intracortically or subcortically depends on whether they lie in barrel or septal columns. To investigate whether this is true for layer V cells, we blocked intracortical activity in the barrel cortex by infusing muscimol from the cortical surface and measuring spike responses to sensory stimulation in the presence of locally iontophoresed bicuculline. Layer V cells beneath barrels had small subcortically generated single- or double-whisker center receptive fields and larger intracortically generated six to seven whisker surround receptive fields. Conversely, septally located cells received multiwhisker input from both subcortical and cortical sources. Most properties of layer Va and layer Vb cells were very similar. However, layer Vb barrel neurons showed a relative lack of phasic inhibition evoked from sensory input compared with layer Va cells. The direct thalamic input to the layer V cells was not sufficient to evoke a sensory response in the absence of input from superficial layers. These findings suggest that despite the apparent overt similarity of layer V receptive fields, barrel and septal subdivisions process different sources of information within the barrel cortex.


2008 ◽  
Vol 100 (2) ◽  
pp. 681-689 ◽  
Author(s):  
Radi Masri ◽  
Tatiana Bezdudnaya ◽  
Jason C. Trageser ◽  
Asaf Keller

In all sensory systems, information is processed along several parallel streams. In the vibrissa-to-barrel cortex system, these include the lemniscal system and the lesser-known paralemniscal system. The posterior medial nucleus (POm) is the thalamic structure associated with the latter pathway. Previous studies suggested that POm response latencies are positively correlated with stimulation frequency and negatively correlated with response duration, providing a basis for a phase locked loop-temporal decoding of stimulus frequency. We tested this hypothesis by analyzing response latencies of POm neurons, in both awake and anesthetized rats, to vibrissae deflections at frequencies between 0.3 and 11 Hz. We found no significant, systematic correlation between stimulation frequency and the latency or duration of POm responses. We obtained similar findings from recording in awake rats, in rats under different anesthetics, and in anesthetized rats in which the reticular activating system was stimulated. These findings suggest that stimulus frequency is not reliably reflected in response latency of POm neurons. We also tested the hypothesis that POm neurons respond preferentially to sensor motion, that is, they respond to whisking in air, without contacts. We recorded from awake, head-restrained rats while monitoring vibrissae movements. All POm neurons responded to passive whisker deflections, but none responded to noncontact whisking. Thus like their counterparts in the trigeminal ganglion, POm neurons may not reliably encode whisking kinematics. These observations suggest that POm neurons might not faithfully encode vibrissae inputs to provide reliable information on vibrissae movements or contacts.


1996 ◽  
Vol 75 (1) ◽  
pp. 217-232 ◽  
Author(s):  
J. Xing ◽  
G. L. Gerstein

1. Mechanisms underlying cortical reorganizations were studied using a three-layered neural network model with neuronal groups already formed in the cortical layer. 2. Dynamic changes induced in cortex by behavioral training or intracortical microstimulation (ICMS) were simulated. Both manipulations resulted in reassembly of neuronal groups and formation of stimulus-dependent assemblies. Receptive fields of neurons and cortical representation of inputs also changed. Many neurons that had been weakly responsive or silent became active. 3. Several types of learning models were examined in simulating behavioral training, ICMS-induced dynamic changes, deafferentation, or cortical lesion. Each learning model most accurately reproduced features of experimental data from different manipulations, suggesting that more than one plasticity mechanism might be able to induce dynamic changes in cortex. 4. After skin or cortical stimulation ceased, as spontaneous activity continued, the stimulus-dependent assemblies gradually reverted into structure-dependent neuronal groups. However, relationships among individual neurons and identities of many neurons did not return to their original states. Thus a different set of neurons would be recruited by the same training stimulus sequence on its next presentation. 5. We also reproduced several typical long-term reorganizations caused by pathological manipulations such as cortical lesions, input loss, and digit fusion. 6. In summary, with Hebbian plasticity rules on lateral connections, the network model is capable of reproducing most characteristics of experiments on cortical reorganization. We propose that an important mechanism underlying cortical plastic changes is formation of temporary assemblies that are related to receipt of strongly synchronized localized input. Such stimulus-dependent assemblies can be dissolved by spontaneous activity after removal of the stimuli.


1994 ◽  
Vol 11 (4) ◽  
pp. 703-720 ◽  
Author(s):  
Ming Sun ◽  
A. B. Bonds

AbstractThe two-dimensional organization of receptive fields (RFs) of 44 cells in the cat visual cortex and four cells from the cat LGN was measured by stimulation with either dots or bars of light. The light bars were presented in different positions and orientations centered on the RFs. The RFs found were arbitrarily divided into four general types: Punctate, resembling DOG filters (11%); those resembling Gabor filters (9%); elongate (36%); and multipeaked-type (44%). Elongate RFs, usually found in simple cells, could show more than one excitatory band or bifurcation of excitatory regions. Although regions inhibitory to a given stimulus transition (e.g. ON) often coincided with regions excitatory to the opposite transition (e.g. OFF), this was by no means the rule. Measurements were highly repeatable and stable over periods of at least 1 h. A comparison between measurements made with dots and with bars showed reasonable matches in about 40% of the cases. In general, bar-based measurements revealed larger RFs with more structure, especially with respect to inhibitory regions. Inactivation of lower cortical layers (V-VI) by local GABA injection was found to reduce sharpness of detail and to increase both receptive-field size and noise in upper layer cells, suggesting vertically organized RF mechanisms. Across the population, some cells bore close resemblance to theoretically proposed filters, while others had a complexity that was clearly not generalizable, to the extent that they seemed more suited to detection of specific structures. We would speculate that the broadly varying forms of cat cortical receptive fields result from developmental processes akin to those that form ocular-dominance columns, but on a smaller scale.


2008 ◽  
Vol 99 (1) ◽  
pp. 356-366 ◽  
Author(s):  
Michael Shoykhet ◽  
Daniel J. Simons

Extracellular single-unit recordings were used to characterize responses of thalamic barreloid and cortical barrel neurons to controlled whisker deflections in 2, 3-, and 4-wk-old and adult rats in vivo under fentanyl analgesia. Results indicate that response properties of thalamic and cortical neurons diverge during development. Responses to deflection onsets and offsets among thalamic neurons mature in parallel, whereas among cortical neurons responses to deflection offsets become disproportionately smaller with age. Thalamic neuron receptive fields become more multiwhisker, whereas those of cortical neurons become more single-whisker. Thalamic neurons develop a higher degree of angular selectivity, whereas that of cortical neurons remains constant. In the temporal domain, response latencies decrease both in thalamic and cortical neurons, but the maturation time-course differs between the two populations. Response latencies of thalamic cells decrease primarily between 2 and 3 wk of life, whereas response latencies of cortical neurons decrease in two distinct steps—the first between 2 and 3 wk of life and the second between the fourth postnatal week and adulthood. Although the first step likely reflects similar subcortical changes, the second phase likely corresponds to developmental myelination of thalamocortical fibers. Divergent development of thalamic and cortical response properties indicates that thalamocortical circuits in the whisker-to-barrel pathway undergo protracted maturation after 2 wk of life and provides a potential substrate for experience-dependent plasticity during this time.


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.


1996 ◽  
Vol 76 (1) ◽  
pp. 371-380 ◽  
Author(s):  
D. W. Adelson ◽  
J. Y. Wei ◽  
L. Kruger

1. Single-unit impulse activity evoked by transient, focal application of hydrogen peroxide (H2O2) to identified visceral receptive fields has been characterized in an in vitro rat splanchnic nerve-mesentery preparation. In addition to H2O2 responsiveness, units were characterized in terms of sensitivity to mechanical stimuli, warming, and bradykinin. 2. Mesenteric receptive fields of single splanchnic afferent C fibers in vitro were located with the use of warm (approximately 45 degrees C saline) or mechanical search stimuli. After delimitation of the warm-sensitive and/or mechanosensitive receptive field, units were tested for responsiveness to transient, focal application of H2O2. Microliter volumes (usually 1 microliter) of H2O2 (88-880 mM) evoked responses in 25 of 42 (60%) units with identified warm-sensitive and/or mechanosensitive receptive fields, and in an additional 10 units for which H2O2 was the only effective stimulus. 3. Tachyphylaxis to repeated H2O2 stimulation was observed with interstimulus intervals <30 min, but did not indicate irreversible inactivation of the terminal, because 1) during this period warm and mechanical stimuli elicited responses equal to or greater than those before H2O2 treatment, and 2) H2O2 sensitivity was restored after units were allowed to recover. 4. Eight units unresponsive to an initial dose of H2O2 responded vigorously to a repeated application at the same site, suggesting a potentiating effect of prior H2O2 exposure. 5. Sixty-two percent (8 of 13) of H2O2-responsive units, but no (0 of 6) H2O2-unresponsive units responded to transient, focal bradykinin (9-90 nM) application. 6. An indirect mode of H2O2-evoked afferent excitation in some units was suggested by several observations, including the prolonged (up to 8 min) duration of the response of some units to transient H2O2 application, and the occasionally long (>2 min) response latencies to focal application of H2O2 to defined receptive fields. 7. Excitation of splanchnic neurons by H2O2 may be relevant to the modulation of reactive oxygen species production by immunocompetent cells, because sensory neuropeptides contained in these afferent fibers are known to influence the respiratory burst of macrophages and neutrophils.


1999 ◽  
Vol 82 (4) ◽  
pp. 1865-1875 ◽  
Author(s):  
P. Wilson ◽  
P. D. Kitchener ◽  
P. J. Snow

The organization of cutaneous receptive fields in the ventroposterior (VP) thalamus of the common marmosets ( Callithrix jacchus) was determined from single-unit recordings, and these data were correlated with the cytochrome oxidase (CO) histochemistry of the thalamus in the same animals. Under continuously maintained ketamine anesthesia, the receptive fields of a total of 192 single units were recorded from the right VP thalamus using 2 MΩ glass microelectrodes. After the receptive fields were mapped, the brains were reacted for CO histochemistry on 50-μm coronal frozen sections through the entire VP thalamus. The majority of units were localized to the CO-reactive regions that define the medial and lateral divisions of VP (VPm and VPl). Apart from the expected finding of the face being represented in VPm and the body in VPl, reconstructing the electrode tracks and unit locations in the histological sections revealed a general association between discrete regions of CO reactivity and the representation of specific body regions. Some low-threshold cutaneous units were apparently localized to VPi (the CO weak regions dorsal, ventral, and interdigitating with, the CO regions of VP). These VPi units were clearly part of the same representational map as the VPl and VPm units. We conclude that the low-threshold cutaneous receptive fields of the marmoset are organized in a single continuous representation of the contralateral body surface, and that this representation can most simply be interpreted as being folded or crumpled into the three-dimensional space of VP thalamus. The folded nature of the body map in VP may be related to the folded nature of VP as revealed by CO histochemistry.


Neuron ◽  
2005 ◽  
Vol 45 (5) ◽  
pp. 781-791 ◽  
Author(s):  
Jon Touryan ◽  
Gidon Felsen ◽  
Yang Dan

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