Extracellular and intracellular recordings from cat's cortical whisker projection area: thalamocortical response transformation

Hellweg, F. C.; Schultz, Wolfram; Creutzfeldt, O. D.

doi:10.1152/jn.1977.40.3.463

Cited by 99 publications

(47 citation statements)

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“…Cortical response adaptation has been observed in a variety of sensory systems after visual (Ohzawa et al, 1982), auditory (Shu Wehr and Zador, 2005), and somatosensory stimuli (Hellweg et al, 1977;Simons, 1985;Gardner et al, 1992). Functionally, adaptation of response magnitude to a sustained stimulus has been suggested as a mechanism for reducing cortical gain, matching neuronal sensitivity to input conditions (Ohzawa et al, 1982;Abbott et al, 1997;Carandini et al, 2002).…”

Section: Discussionmentioning

confidence: 99%

Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation

Higley¹,

Contreras²

2006

J. Neurosci.

252

244

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In layer 4 (L4) of the rat barrel cortex, a single whisker deflection evokes a stereotyped sequence of excitation followed by inhibition, hypothesized to result in a narrow temporal window for spike output. However, awake rats sweep their whiskers across objects, activating the cortex at frequencies known to induce short-term depression at both excitatory and inhibitory synapses within L4. Although periodic whisker deflection causes a frequency-dependent reduction of the cortical response magnitude, whether this adaptation involves changes in the relative balance of excitation and inhibition and how these changes might impact the proposed narrow window of spike timing in L4 is unknown. Here, we demonstrate for the first time that spike output in L4 is determined precisely by the dynamic interaction of excitatory and inhibitory conductances. Furthermore, we show that periodic whisker deflection results in balanced adaptation of the magnitude and timing of excitatory and inhibitory input to L4 neurons. This balanced adaptation mediates a reduction in spike output while preserving the narrow time window of spike generation, suggesting that L4 circuits are calibrated to maintain relative levels of excitation and inhibition across varying magnitudes of input.

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Section: Discussionmentioning

confidence: 99%

Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation

Higley¹,

Contreras²

2006

J. Neurosci.

252

244

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“…The larger distance of hyperpolarization from the center of activity can assist in explaining the underlying cortical dynamics responsible for generating the phenomena of surround inhibition and cutaneous masking in single cortical cells (Hellweg et al, 1977;Laskin and Spencer, 1979;Simons and Carvell, 1989). However, we do not know whether the stronger hyperpolarization detected at the periphery reflects stronger peripheral inhibition rather than a strong center inhibition masked by a larger center depolarization.…”

Section: The Surround Hyperpolarizationmentioning

confidence: 95%

“…Such a pattern is seen in extracellular studies (Laskin and Spencer, 1979;Simons and Carvell, 1989), in intracellular studies (Andersson, 1965;Hellweg et al, 1977;Carvell and Simons, 1988;Zhu and Connors, 1999), and in voltage-sensitive dye (VSD) studies (Orbach et al, 1985;Kleinfeld and Delaney, 1996;Takashima et al, 2001). …”

Section: Introductionmentioning

confidence: 94%

Imaging Spatiotemporal Dynamics of Surround Inhibition in the Barrels Somatosensory Cortex

et al. 2003

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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 ϳ16 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.

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“…The most salient observation was that the dynamics exhibited by cortical neurons while adapting to the stimulus train were both layer specific and stimulus specific. Typically, when applying repetitive stimulations to passive sensory organs, cortical responses depress (Mountcastle et al, 1957;Hellweg et al, 1977;Simons, 1978;Ulanovsky et al, 2004). With our active stimulation paradigm, responses to stimuli presented at similar frequencies and producing similar initial responses either facilitated, did not change, or depressed, depending on the sensory information conveyed (i.e., presence or absence of an object) and on the cortical layer.…”

Section: Introductionmentioning

confidence: 92%

Layer-Specific Touch-Dependent Facilitation and Depression in the Somatosensory Cortex during Active Whisking

Derdikman¹,

Yu²,

Haidarliu³

et al. 2006

J. Neurosci.

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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 ϳ1 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.

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Extracellular and intracellular recordings from cat's cortical whisker projection area: thalamocortical response transformation

Cited by 99 publications

References 0 publications

Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation

Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation

Imaging Spatiotemporal Dynamics of Surround Inhibition in the Barrels Somatosensory Cortex

Layer-Specific Touch-Dependent Facilitation and Depression in the Somatosensory Cortex during Active Whisking

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