Intracortical Excitation of Spiny Neurons in Layer 4 of Cat Striate Cortex In Vitro

Abstract

Recordings were made from pairs of neurons in cat striate visual cortex in vitro to study the AMPA-channel-mediated components of intracortical excitatory synaptic connections between layer 4 spiny neurons and between layer 6 and layer 4 spiny neurons. Forty-six of the 72 cells recorded were identified morphologically. They consisted of spiny stellate and pyramidal cells in layer 4, and pyramidal cells in layer 6. Connections between layer 4 excitatory cells involve excitatory postsynaptic potentials (EPSPs) averaging 949 microV, with an average coefficient of variation of 0.21 (n = 30). The synapses operate at very high release probabilities (0.69-0.98). With repetitive stimulation these EPSPs show varying degrees of depression, largely mediated by presynaptic changes in release probability. Four pairs of layer 4 cells were reciprocally connected. The connections from layer 6 to layer 4 involve smaller, more variable EPSPs, with an average amplitude of 214 microV, and average coefficient of variation 0.72 (n = 7). These synapses operate at moderately high release probabilities (0.37-0.56). They show facilitation with repetitive stimulation, mediated largely by presynaptic changes in release probability. One excitatory connection from a layer 4 neuron to a layer 6 pyramidal cell was also detected. Thus, layer 4 spiny neurons receive effective excitation from two intracortical sources that have different synaptic dynamics and are likely to contribute significantly to the temporal properties of these cells in vivo.

Functional organization of excitatory synaptic strength in primary visual cortex

“…A total of 203 pyramidal cells (across 17 mice) recorded in the slice were identified in the in vivo image stacks, and the overall connection rate was 75/520 (0.14). Consistent with previous reports [1][2][3][4][5][6][7][8][9] , the distribution of excitatory postsynaptic potential (EPSP) amplitudes was highly skewed (median EPSP amplitude: 0.19 mV; mean EPSP amplitude ± s.d. : 0.45 ± 0.68 mV; Fig.…”

“…Excitatory connection amplitudes between pairs of cortical neurons vary over two orders of magnitude, comprising only very few strong connections among many weaker ones [1][2][3][4][5][6][7][8][9] . Although this highly skewed distribution of connection strengths is observed in diverse cortical areas 1-9 , its functional significance remains unknown: it is not clear how connection strength relates to neuronal response properties, nor how strong and weak inputs contribute to information processing in local microcircuits.…”

“…We describe a simple rule governing how the long-tailed distribution of excitatory connection strength -observed in diverse cortical areas [1][2][3][4][5][6][7][8][9] -is organized with respect to the functional properties of cortical neurons. In L2/3 of mouse V1, pyramidal neurons with correlated responses to visual stimuli connect preferentially with strong and often reciprocal connections, whereas neurons with uncorrelated or anti-correlated responses connect infrequently with weak connections.…”

Synaptic Responses to Whisker Deflections in Rat Barrel Cortex as a Function of Cortical Layer and Stimulus Intensity

“…The first mechanism could play a role if layer 4 circuits are more compact than SGr or IGr circuits. However, the responses we recorded receive a large contribution of local circuit activity from different sources (Tarczy-Hornoch et al, 1999;Martin, 2002;Schubert et al, 2003) making predictions about the electrotonic distribution of the input very difficult. The second mechanism is supported in part by the highly synchronized input from thalamus to layer 4 at the highest velocity (Pinto et al, 2000), which has a high efficacy (Gil 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

“…In analogy to the visual cortex, spiny layer 4 neurons may also establish synaptic contacts with layer 6 pyramidal neurons and in turn may receive synapses from these neurons (Gilbert and Wiesel, 1979;Martin and Whitteridge, 1984;McGuire et al, 1984;Benshalom and White, 1986;Ahmed et al, 1994;Stratford et al, 1996;Tarczy-Hornoch et al, 1999). The axonal projection of spiny layer 4 neurons toward layer 6 makes it likely that such a feed-forward A functional cortical column is superimposed in light gray.…”