Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Neuronal Diversity and Temporal Dynamics

 

Science 4 July 2008: Vol. 321. no. 5885, pp. 53 - 57

Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations

Thomas Klausberger^1,2 and Peter Somogyi¹

¹ MRC Anatomical Neuropharmacology Unit, Oxford University, Oxford OX1 3TH, UK.
² Center for Brain Research, Medical University of Vienna, A-1090 Vienna, Austria.

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In the cerebral cortex, diverse types of neurons form intricate circuits and cooperate in time for the processing and storage of information. Recent advances reveal a spatiotemporal division of labor in cortical circuits, as exemplified in the CA1 hippocampal area. In particular, distinct GABAergic (-aminobutyric acid–releasing) cell types subdivide the surface of pyramidal cells and act in discrete time windows, either on the same or on different subcellular compartments. They also interact with glutamatergic pyramidal cell inputs in a domain-specific manner and support synaptic temporal dynamics, network oscillations, selection of cell assemblies, and the implementation of brain states. The spatiotemporal specializations in cortical circuits reveal that cellular diversity and temporal dynamics coemerged during evolution, providing a basis for cognitive behavior.

The cerebral cortex of mammals has a large diversity of cells operating in intricate circuits. This cellular diversity endows the cerebral cortex with the capacity to perform complex biological processes such as the subjective representation and interpretation of the world, encoding and retrieval of emotionally colored memories, understanding and empathizing with other individuals, and scientifically investigating the universe (including the mind).

The CA1 area of the hippocampus constitutes one of the simplest and most examined cortical areas where recent progress has been made in explaining neuronal diversity and the temporal activity of distinct cells. Here, excitatory pyramidal cells encode representations of spatial (2) and other episodic memories (3) and provide glutamatergic output to other cortical as well as subcortical areas.

The relatively uniform pyramidal cells are supported by a rich diversity of GABAergic interneurons that provide general inhibition and also temporally regulate pyramidal cell activity.

The dynamic timing of synaptic action between different types of interneuron and pyramidal cells supports distinct brain states and cognitive processing.

A CA1 pyramidal cell receives about 30,000 synaptic inputs and emits several types of dendrite to provide a framework for their integration. The cell body integrates inputs from the dendrites and receives only GABAergic synapses, as does the axon-initial segment, which contributes to action potential generation. The small, oblique dendrites emerging from one or two large apical dendrites and the basal dendrites receive glutamatergic input mainly from the hippocampal CA3 area, local axon collaterals, and the amygdala. The apical dendritic tuft is innervated mainly by glutamatergic inputs from the entorhinal cortex and the thalamus. All dendrites also receive local GABAergic inputs from interneurons.

Network oscillations in the cerebral cortex indicate highly coordinated neuronal activity (14) over large areas. For example, theta oscillations (4 to 10 Hz) highlight the online state of the hippocampus and related structures. Theta waves together with gamma oscillations (30 to 80 Hz) occur during spatial navigation, memory tasks, and rapid-eye-movement sleep. In contrast, sharp wave-associated ripples (100 to 200 Hz) occur during resting, consummatory behavior, and slow-wave sleep, supporting offline replay and consolidation of previous experiences.

Because these different interneurons innervate distinct domains of pyramidal cells, they imprint a spatiotemporal GABAergic conductance matrix onto the pyramidal cells. This GABAergic fingerprint changes its pattern during different brain states.

Many distributed areas of the cerebral cortex participate in each cognitive process. Coordination is supported by shared subcortical pathways and by inter-areal pyramidal cell projections terminating on both pyramidal cells and local GABAergic interneurons.

Because these projection cells fire rhythmically during sharp wave-associated ripple and gamma oscillations, they contribute to temporal organization across the septohippocampal-subicular circuit.

Information between cortical areas is transmitted via axonal projections of glutamatergic pyramidal cells, but they alone may not produce the required high degree of temporal precision between brain regions. Together with common subcortical state-modulating inputs, the cortical long-range GABAergic projections could prime and reset activity in specific neurons of the target areas before the information arrives via glutamatergic fibers from pyramidal cells. The neuronal diversity of GABAergic projection neurons differing in target area and temporal activity increases computational powers between related cortical areas.

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