Pyramidal cell communication within local networks in layer 2/3 of rat neocortex

Abstract

Communication relies on the use of a common system of signs or behaviours. Within the neocortex this occurs through the exchange of information locally and interareally using neuronal code in the form of spike trains. Pyramidal cell communication in layer 2/3 represents the response of these cells to afferent and local network signals. The role of local pyramidal cells in the shaping of pyramidal cell firing is determined by their functional connectivity. This process presumably underlies information processing within the neocortex, the understanding of which is one of the principal goals of modern neuroscience. The extent to which neocortical pyramidal cells function as a local network is determined by the strength and probability of their connections. By mapping connections between pyramidal cells we show here that in a local network of about 600 pyramidal cells located within a cylindrical volume of 200 mm w 200 mm of neocortical layer 2/3, an individual pyramidal cell receives synaptic inputs from about 30 other pyramidal neurons, with the majority of EPSP amplitudes in the 0.2-1.0 mV range. The probability of connection decreased from 0.09 to 0.01 with intercell distance (over the range 25-200 mm). Within the same volume, local interneuron (fast-spiking non-accomodating interneuron, FS)-pyramidal cell connections were about 10 times more numerous, with the majority of connections being reciprocal. The probability of excitatory and inhibitory connections between pyramidal cells and FS interneurons decreased only slightly with distance, being in the range 0.5-0.75. Pyramidal cells in the local network received strong synaptic input during stimulation of afferent fibres in layers 1 and 6. Minimal-like stimulation of layer 1 or layer 6 inputs simultaneously induced postsynaptic potentials in connected pyramidal cells as well as in pyramidal-FS cell pairs. These inputs readily induced firing of pyramidal cells, although synaptically connected cells displayed different firing patterns. Unitary EPSPs in pyramidal-pyramidal cell pairs did not detectably alter cell firing. FS interneurons fire simultaneously with pyramidal cells. In pyramidal-FS cell pairs, both unitary EPSPs and IPSPs efficiently modulated cell firing patterns. We suggest that computation in the local network may proceed not only by direct pyramidal-pyramidal cell communication but also via local interneurons. With such a high degree of connectivity with surrounding pyramidal cells, local interneurons are ideally poised to both coordinate and expand the local pyramidal cell network via pyramidal-interneuron-pyramidal communication.

Functional organization of excitatory synaptic strength in primary visual cortex

“…5). Connections between bidirectionally connected pairs generated larger EPSPs than unidirectionally connected pairs, consistent with previous reports 3,4,17 , and the RF maps of bidirectionally connected neurons were significantly more correlated than RFs of unidirectionally connected or unconnected pairs (Extended Data Fig. 5).…”

“…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.…”

Sensory experience modifies spontaneous state dynamics in a large-scale barrel cortical model

“…Specifically, Holmgren et al (2003) Izhikevich & Edelman (2008). The entries with asterisks are taken from Lefort et al (2009 reported a decrease from 9% probability of two cells within ± 25 µm of each other being connected, to 1% at distances > 100 µm for p II/III -p II/III synapses in visual and somatosensory cortex.…”