Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat

P. Somogyi, Z. F. Kisvárday, K. A.C. Martin, D. Whitteridge

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Abstract

Neurons were studied in the striate cortex of the cat following intracellular recording and iontophoresis of horseradish peroxidase. The three selected neurons were identified as large basket cells on the basis that (i) the horizontal extent of their axonal arborization was three times or more than the extent of the dendritic arborization; (ii) some of their varicose terminal segments surrounded the perikarya of other neurons. The large elongated perikarya of the first two basket cells were located around the border of layers III and IV. The radially-elongated dendritic field, composed of beaded dendrites without spines, had a long axis of 300-350 μm, extending into layers III and IV, and a short axis of 200 μm. Only the axon, however, was recovered from the third basket cell. The lateral spread of the axons of the first two basket cells was 900 μm or more in layer III and, for the third cell, was over 1500 μm in the antero-posterior dimension, a value indicating that the latter neuron probably fulfills the first criterion above. The axon collaterals of all three cells often branched at approximately 90° to the parent axon. The first two cells also had axon collaterals which descended to layers IV and V and had less extensive lateral spreads. The axons of all three cells formed clusters of boutons which could extend up a radial column of their target cells. Electron microscopic examination of the second basket cell showed a large lobulated nucleus and a high density of mitochondria in both the perikarya and dendrites. The soma and dendrites were densely covered by synaptic terminals. The axons of the second and third cells were myelinated up to the terminal segments. A total of 177 postsynaptic elements was analysed, involving 66 boutons of the second cell and 89 boutons of the third cell. The terminals contained pleomorphic vesicles and established symmetrical synapses with their postsynaptic targets. The basket cell axons formed synapses principally on pyramidal cell perikarya (approximately 33% of synapses), spines (20% of synapses) and the apical and basal dendrites of pyramidal cells (24% of synapses). Also contacted were the perikarya and dendrites of non-pyramidal cells, an axon, and an axon initial segment. A single pyramidal cell may receive input on its soma, apical and basal dendrites and spines from the same large basket cell. Seven pyramidal neurons that were postsynaptic to the second and third identified basket cells received synaptic contacts on their soma (average of 4.4 from one basket cell) and proximal dendrites (average 2.3). The results provide evidence that large basket cells establish multiple synaptic contacts with the neurons they seem to select as postsynaptic targets. At least 30% or more of their postsynaptic targets are the perikarya of other neurons. In the light of recent immunocytochemical studies on the visual cortex of the cat, large basket cells may use γ-aminobutyrate as their transmitter and they are probably inhibitory in function. Since large basket cells also contact dendrites and spines, their effect cannot be explained by a simple somatic inhibitory mechanism and their functional role must also be considered in relation to other inputs to different parts of the same neuron. The structural features of large basket cells are compared with those of other putative inhibitory interneurons and their role in the functioning of the visual cortex is discussed.

Original languageEnglish
Pages (from-to)261-294
Number of pages34
JournalNeuroscience
Volume10
Issue number2
DOIs
Publication statusPublished - Oct 1983

ASJC Scopus subject areas

  • Neuroscience(all)

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