Distributed representation of vibrissa movement in the upper layers of somatosensory cortex revealed with voltage-sensitive dyes

Abstract

We have identified large-scale patterns of electrical activity in circuits that occur in response to stimulation of peripheral receptors. Our focus was on primary (S1) vibrissal cortex of anesthetized rat, and we used optical techniques in conjunction with voltage-sensitive dyes to measure depolarization of the upper layers of cortex. Displacement of one vibrissa produced a field of activity that extends over very many cortical columns in S1. There are multiple, focal maxima within this field. A global maximum is located near the center of the field of activity, and, as determined electrically and histologically, this site maps to the cortical column appropriate for the deflected vibrissa. The amplitude of this component attains a steady-state value under continuous stimulation. Additional temporal characteristics are revealed by the response to a single displacement; the signal was triphasic and began with a prompt depolarization that was followed by a transient phase of inhibition and a final phase of long-lasting depolarization. The somatotopy of the other, satellite maxima in the field of activity were established through the reconstruction of the fields of activity produced by individual stimulation of other vibrissae. Local maxima for one vibrissa were seen to overlie the global maximum found for stimulation of nearest- and next-nearest-neighbor vibrissae. In contrast to the amplitude of the global maxima, the amplitude associated with the local maxima was not maintained with either continuous or infrequent but repetitive stimulation. Finally, the field of activity induced by alternate deflection of two neighboring vibrissae was suppressed in amplitude in comparison to the summed amplitudes of the signals elicited by deflection of each vibrissa alone. We suggest that these patterns of activity are a manifestation of the dynamic interaction among neighboring cortical columns.

Imaging Spatiotemporal Dynamics of Surround Inhibition in the Barrels Somatosensory Cortex

“…This finding, using a variety of stimulus types, is in congruence with the findings of Petersen et al (2003), in which it is also shown by histology that the VSD activity originates at the center of the corresponding barrel (Kleinfeld and Delaney, 1996).…”

“…2, 4) and by Takashima et al (2001). In contrast, Kleinfeld and Delaney (1996) detected a triphasic response, but without the net hyperpolarization.…”

“…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). …”

“…To study temporal patterns of populations of neurons (rather than single cells) and to map the loci of excitation, suppression, and net hyperpolarization across the cortical surface, we used in vivo VSDI (voltage-sensitive dye imaging) (Grinvald et al, 1984), which had already proved to be useful in exploring cortical dynamics in the visual cortex of cats and monkeys (Arieli et al, 1996;Tsodyks et al, 1999;Slovin et al, 2002) and in the somatosensory cortex of rats (Orbach et al, 1985;Kleinfeld and Delaney, 1996). Recent intracellular recordings in vivo in deeply anesthetized cats (A. Sterkin, I. Lampl, D. Ferster, D. E. Glaser, A. Grinvald, and A Arieli, unpublished observations) (Grinvald et al, 1999, their Fig.…”

Columnar Organization of Dendrites and Axons of Single and Synaptically Coupled Excitatory Spiny Neurons in Layer 4 of the Rat Barrel Cortex

“…This may represent the initial step in the cortical integration of afferent sensory signals from several whiskers. This proposal is supported by in vivo 2-deoxyglucose mapping and imaging studies showing that the tangential spread of excitation occurs indeed at the level of layer 2/3 (McCasland and Woolsey, 1988;Kleinfeld and Delaney, 1996;Woolsey et al, 1996). Finally, layer 2/3 pyramidal cells can excite layer 5 pyramidal cells, the principal output neurons of the neocortex (Thomson and Bannister, 1998;Reyes and Sakmann, 1999).…”