Phasic loss of constraints in timing of neuronal spikes in the feline centrum medianum during EEG alpha-like activity

Abstract

In unrestrained cats, temporal patterns of single neuronal firing in the centrum medianum-parafascicular complex (CM-Pf) of thalamus were studied during a state of motionless quiet wakefulness. The spike trains from each neuron were electronically divided into episodes that occurred during desynchronized EEG and those that occurred during bursts of 6–14 Hz EEG spindles or alpha-like activity over the parieto-occipital cortex and in the CM-Pf. Contrary to expectations based on the theory of inhibitory phasing of neuronal activity, the episodes of synchronized quiet wakefulness (S-QW) were associated with independent and random distribution of spike intervals, although they tended to occur in clusters. During episodes of desynchronized quiet wakefulness (D-QW), significant temporal patterns were emitted by most neurons studied. The results suggest that: (a) during D-QW and increased levels of vigilance, temporal patterns are generated by cognitive processes and enhanced specific connectivities between CM-Pf neurons and other systems; (b) if connectivity is defined as increased certainty of synaptic transmission and iterative activation of the same pathways, then the assumption that the gross EEG thalamo-cortical synchronization represents increased connectivities between the CM-Pf neurons and other systems, may be erroneous; and (c) since temporal patterns of single neuronal discharges are determined by specific spatio-temporal distribution of synaptic drive, therefore during EEG spindles, most EPSP-IPSP sequences impinging upon CM-Pf neurons are conveyed by randomly varying polysynaptic pathways and have random spatio-temporal distribution on the soma and dendrites. In light of other observations, such a process is equivalent to an active introduction of uncertainty or ‘entropy’ into the information processing system, a state which may be important in preserving plasticity of operational modes of CM-Pf neurons and those with which they directly and/or indirectly interact.