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Journal of Neuroscience, Vol 10, 508-519, Copyright © 1990 by Society for Neuroscience
Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum
CJ Wilson, HT Chang and ST Kitai
Department of Anatomy and Neurobiology, University of Tennessee, Memphis College of Medicine 38163.
Intracellular recordings were made in vivo from 9 giant aspiny neurons in
the neostriatum of urethane-anesthetized rats. The cells were identified by
intracellular staining with HRP or biocytin. The neurons exhibited
morphological features typical of neostriatal cholinergic interneurons. Six
of the cells were obtained from intact animals, while 3 were recorded from
rats with ipsilateral hemidecortications. Giant aspiny neurons were
characterized by their slow irregular but tonic (3- 10/sec) spontaneous
activity and long-duration action potentials. Examination of the underlying
membrane potential trajectories during spontaneous firing revealed that
individual action potentials were triggered from spontaneous small (1-5 mV)
depolarizing potentials. These spontaneous potentials exhibited the voltage
sensitivity of ordinary EPSPs. They were much less frequent during the
80-200 msec pause in tonic afferent input that follows the excitation
evoked by cortical or thalamic stimulation, and were decreased in frequency
in decorticate animals. Their rise times and half-widths matched those
expected for unitary synaptic potentials placed proximally on the surface
of the neurons. Low-intensity stimulation of neostriatal afferents produced
small short-latency EPSPs that appeared to be composed of responses
identical to the spontaneous depolarizing potentials. The latencies of the
EPSPs evoked from the cerebral cortex and thalamus were consistent with a
monosynaptic input from both structures, but the maximal size of the EPSPs
was much smaller than that evoked in spiny neurons, suggesting that a
smaller number of afferent inputs make synapses with each of the aspiny
cells. Giant aspiny neurons exhibited much larger input resistances and
longer time constants than spiny neostriatal neurons. They also exhibited
relatively linear steady-state current-voltage relationship compared to
spiny projection cells. Input resistances ranged from 71-105 M omega, and
time constants ranged from 17.8-28.5 msec. Analysis of the charging
transients in response to current pulses yielded estimates of dendritic
length of approximately 1 length constant. Repetitive firing of the neurons
was limited by a powerful spike afterhyperpolarization and by a strong
spike frequency adaptation. The sensitivity of the giant aspiny interneuron
to a relatively small number of proximal afferent synaptic contacts, its
tonic firing, and its widespread dendritic and axonal fields place it in an
excellent position to act as a modulator of the excitability of neostriatal
projection neurons in advance of the onset of movement-related neostriatal
activity.
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