Limits to the temporal fidelity of cortical spike rate signals.

The cerebral cortex processes information primarily through changes in the spike rates of neurons within local ensembles. To evaluate how reliably the average spike rate of a group of cortical neurons can represent a time-varying signal, we simulated an ensemble with realistic spike discharge behavior. We found that weak interneuronal correlation, or synchrony, allows the variability in spike rates of individual neurons to compromise the ensemble representation of time-varying signals. Brief cycles of sinusoidal modulation at frequencies above 115 Hz could not be represented by an ensemble of hundreds of neurons whose interneuronal correlation mimics that of the visual cortex. The spike variability and correlation assumed in our simulations are likely to apply to many areas of cortex and therefore may constrain the fidelity of neural computations underlying higher brain function.

Interhemispheric coordination of premotor neural activity during singing in adult zebra finches.

The song system, a neural network that mediates the learning and production of song by oscine songbirds, is investigated extensively as a model system for understanding the neural basis of complex skill learning. Part of the complexity of birdsong arises from the coordinated recruitment of multiple groups of muscles on both sides of the body. Although the song system is bilaterally organized, little is known about how premotor activities on the two sides are coordinated during singing. We investigated this by unilaterally recording neural activity in the forebrain song nucleus HVc (also known as the high vocal center) during singing and by forcing the premotor activities in the two hemispheres out of synchrony by perturbing neural activity in the contralateral HVc with electrical stimulation. Perturbing the activity in one HVc at any time during a song led to a short-latency readjustment of activity in the contralateral HVc. This readjustment consisted of a true resetting of the temporal pattern of activity in the contralateral HVc rather than merely a transient activity suppression overlaid on an unaltered pattern of premotor activity. These results strongly suggest that the output of song premotor areas in the forebrain is continuously monitored and that an active mechanism exists for resynchronizing the outputs from the two hemispheres whenever their gross temporal patterns differ significantly. The possible anatomical substrates for these coordinating mechanisms and their potential roles in song learning are discussed.

Identification of a forebrain motor programming network for the learned song of zebra finches.

The stereotyped delivery of sequences of vocalizations by singing zebra finches is thought to be mediated by a "central motor program." We hypothesized that electrically stimulating, and thus perturbing, the neural components of this motor program during singing should alter the subsequent singing pattern. In contrast, perturbing the activity of other neurons in the song motor pathway that do not participate directly in generating the song temporal pattern should not affect the singing pattern. We found that unilaterally stimulating the forebrain area RA of singing birds with chronically implanted electrodes distorted ongoing syllables without changing the order or timing of ensuing syllables. However, stimulating forebrain area HVc, which projects directly to RA, altered both ongoing syllables and the ensuing song pattern. These findings indicate that syllable sequencing during singing is organized in forebrain areas above RA (including HVc) and that the resulting pattern is imposed on lower structures of the motor pathway. Furthermore, the observation that unilateral forebrain perturbation was sufficient to alter the pattern of this bilaterally organized behavior suggests that (non-auditory) feedback pathways to the forebrain exist to coordinate the two hemispheres during singing. We suggest that the study of the motor control system for birdsong has provided the most direct evidence to date for localizing the programming of a skilled motor sequence to the telencephalon.