Physiology and Morphology of Intratelencephalically Projecting Corticostriatal-Type Neurons in Pigeons as Revealed by Intracellular Recording and Cell Filling

Abstract

Much of the Wulst and dorsal ventricular ridge (DVR) in birds, which together make up the part of the avian telencephalon functionally resembling mammalian cerebral cortex, projects to the striatum. Those connections arise from neurons projecting additionally to the brainstem as well as from neurons projecting only within the telencephalon. As part of an effort to further characterize corticostriatal-type projection neurons in birds, we recorded intracellularly from neurons of the outer DVR, identified neurons projecting to the striatum by antidromic stimulation from the ipsilateral rostromedial striatum or subsequently by their axonal projection, characterized these neurons physiologically and then filled them with biocytin. As neurons in the outer DVR only project within telencephalon, neurons within it projecting to the striatum are of the intratelencephalically projecting (IT) type. Our studies suggest that: (1) the membrane potentials of avian IT-type neurons fluctuate between two preferred subthreshold values, and action potentials occur only in the ‘up’ state, (2) avian IT-type neurons show a time-dependent inward rectification in response to hyperpolarization and regular firing in response to constant current injection, (3) the conduction velocity of avian IT-type neurons is slow (about 0.2 m/s), (4) avian IT-type neurons possess radially disposed densely spiny dendrites but no apical dendrite, (5) avian IT-type neurons have local and distant collateral projections within the DVR, and (6) individual avian IT-type neurons give rise to an extensive terminal field within the striatum. Aside from the shape of their dendritic tree, IT-type neurons in birds closely resemble IT-type corticostriatal neurons in mammals in these various aspects, although it is presently uncertain whether this neuron type has been inherited in common by birds and mammals from stem amniotes.

Cellular Localization of AMPA Type Glutamate Receptor Subunits in the Basal Ganglia of Pigeons <i>(Columba livia)</i>

“…The corticostriatal input in mammals imparts a two-state behavior to striatal projection neurons, with spiking in response to cortical stimulation occurring from a slightly depolarized up state [Wilson, 1993;Wilson and Kawaguchi, 1996]. This two-state behavior has been demonstrated in corticostriatal projection neurons in pigeons as well [Reiner et al, 2001], thus suggesting that cortical input to avian striatal projection neurons may impart to them via AMPA receptors the same two-state behavior observed in mammalian striatal projection neurons. As in mammals, the AMPA receptors involved in such responses appear to consist in birds primarily of GluR2 in combination with GluR1 and/or GluR3.…”

Long-Term Potentiation in an Avian Basal Ganglia Nucleus Essential for Vocal Learning

“…In addition to providing necessary presynaptic activation, this high-frequency activity may contribute to strong postsynaptic depolarization. Another source of prolonged postsynaptic depolarization could be the synaptically driven "up" states, as described in mammalian striatum and avian corticostriatal-like neurons in vivo (Wilson and Groves, 1981;Wilson and Kawaguchi, 1996;Reiner et al, 2001). A combination of the three necessary components (i.e., presynaptic activity, postsynaptic depolarization, and activation of DA receptors) can enable LTP induction at the glutamatergic synapses in area X in vivo.…”

Plumes of neuronal activity propagate in three dimensions through the nuclear avian brain

“…In mammals, each cycle of a traveling slow-wave (that is, an EEG peak) is thought to reflect one up-state, spreading from a site of origin to neighboring regions. Given the limited data on trans-membrane potentials during NREM sleep or anesthesia in birds, it is not possible to say whether multiple plumes arise and propagate during a single up-state or whether one propagating plume corresponds to one short up-state; although the former seems more likely given the single report of slow-oscillations in birds [19] and the duration of avian EEG slow-waves. Furthermore, it is difficult to conclude whether or not the situation of multiple-propagating-plumes-per-presumed-up-state that we find in birds is different from the one-traveling-wave-per-up-state situation described in mammals.…”

“…To distinguish between these alternatives, we studied brain activity in birds, the only non-mammalian group known to exhibit slow-oscillations [19] and associated EEG slow-waves comparable to those observed in mammals during NREM sleep [20,21]. This similarity between mammals and birds is particularly interesting because unlike the laminar mammalian neocortex, neurons in the avian forebrain are arranged in a largely nuclear manner [22].…”