Thalamic-Evoked Synaptic Interactions in Barrel Cortex Revealed by Optical Imaging

Abstract

We used optical imaging of voltage-sensitive dye signals to study the spatiotemporal spread of activity in the mouse barrel cortex, evoked by stimulation of thalamocortical afferents in an in vitro slice preparation. Stimulation of the thalamus, at low current intensity, results in activity largely restricted to a single barrel, and to the border between layers Vb and VI. Low concentrations of the GABA A receptor antagonist bicuculline increase the amplitude of the optical signals, without affecting their spatiotemporal propagation. Higher concentrations of bicuculline result in paroxysmal activity, which propagates via intracolumnar and intercolumnar excitatory pathways. Enhancing the activity of NMDA receptors, by removing Mg 2ϩ from the extracellular solution, dramatically alters the spatiotemporal pattern of excitation: activity spreads to supragranular and infragranular layers and adjacent barrel columns. This enhanced propagation is suppressed by the NMDA receptor antagonist AP5. A similar enhancement of activity propagation can be produced by stimulating the thalamus with a short, high-frequency pulse train. Application of AP5 suppresses the frequency-dependent spread of activity. These findings indicate that the spatiotemporal spread of activity in the barrel cortex is altered by varying the temporal patterns of thalamic inputs, via an NMDA receptor-mediated mechanism, and suggest that a similar process occurs during repetitive whisking activity. Key words: somatosensory cortex; voltage-sensitive dyes; glutamate; NMDA; GABA; epilepsy; temporal coding; mouseProcessing of sensory information in the cerebral cortex can be described as a hierarchical process, in which inputs from "specific" thalamic nuclei are integrated by their postsynaptic cortical targets, which, in turn, provide inputs to neurons in other layers of the same functional column and subsequently to adjacent columns (Gilbert, 1992;Keller, 1995;Rauschecker et al., 1997). Although this hierarchical scheme is oversimplified in that it omits factors such as parallel processing and feedback interactions, it is thought to faithfully represent at least the initial stages of cortical sensory processing (Stone et al., 1979;Felleman and Van Essen, 1991;Iwamura, 1993).To understand the mechanisms underlying cortical sensory processing, it is necessary to determine how thalamic inputs are integrated by their postsynaptic cortical neurons and propagated via intracolumnar and intercolumnar cortical pathways. This requires methods to identify discrete functional columns and to reveal the spatiotemporal propagation of thalamic inputs within and among these columns. In the present study we took advantage of a functional imaging approach (see Orbach and Cohen, 1983;Cinelli and Salzberg, 1987;Yuste et al., 1997;Keller et al., 1998) to investigate intracortical processing of thalamic inputs in the somatosensory cortex and its modulation by glutamatergic and GABAergic processes.The somatosensory cortex of certain rodent species contains representations of the my...

The Role of Thalamic Inputs in Surround Receptive Fields of Barrel Neurons

“…Sparse intercolumnar connections also target the supragranular branches of apical dendrites belonging to layer IV star pyramids (Schubert et al, 2003), and these mediate weak synaptic interactions (Feldmeyer et al, 1999;Petersen and Sakmann, 2000;Schubert et al, 2003). In addition, analyses of voltagesensitive dye signals fail to demonstrate direct interbarrel pathways (Laaris et al, 2000;Laaris and Keller, 2002;Petersen et al, 2003). Finally, under the light narcosis used here, AW responses are unaffected by lesions of adjacent barrels (Goldreich et al, 1999).…”

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

“…This finding is further supported by optical recordings of voltage-sensitive dyes, which have shown that excitatory activity evoked by stimulation of thalamocortical afferents is largely restricted to a single barrel whereas in layer 2/3 it spreads across cortical columns (Laaris et al, 2000). It may be speculated that in layer 2/3 excitation arriving from layer 4 is distributed by pyramidal cell axons throughout the primary somatosensory cortex in vertical and horizontal directions (for review, see DeFelipe and Farinas, 1992).…”

Differential Columnar Processing in Local Circuits of Barrel and Insular Cortices

“…3). Thus, the intercolumnar synchronization in layer II/III seems to be strictly controlled by GABA A inhibition (Laaris et al, 2000;Petersen and Sakmann, 2001;Laaris and Keller, 2002), which is likely to operate in a feedforward manner after activation of layer II/III pyramidal neurons in the home column by the inputs arising from layer IV.…”

“…In the rodent barrel cortex, a distinct topographical representation of the whisker is well known (Woolsey and Van der Loos, 1970;Moore et al, 1999), and the presence of columnar organization is most apparent in this area as revealed by the barrel structure of layer IV (Feldmeyer et al, 1999(Feldmeyer et al, , 2005Laaris et al, 2000;Lubke et al, 2000;Sakmann, 2000, 2001;Bender et al, 2003). In contrast, in the primary gustatory area of the insular cortex, the topographical representation of the four basic tastes (sweet, sour, salty, and bitter) appears to be much less distinct (Yamamoto et al, 1980(Yamamoto et al, , 1984(Yamamoto et al, , 1985Kosar et al, 1986;Ogawa et al, 1991Ogawa et al, , 1992.…”