Inhibitory Network Interactions Shape the Auditory Processing of Natural Communication Signals in the Songbird Auditory Forebrain

Abstract

The role of GABA in the central processing of complex auditory signals is not fully understood. We have studied the involvement of GABA A-mediated inhibition in the processing of birdsong, a learned vocal communication signal requiring intact hearing for its development and maintenance. We focused on caudomedial nidopallium (NCM), an area analogous to parts of the mammalian auditory cortex with selective responses to birdsong. We present evidence that GABA A-mediated inhibition plays a pronounced role in NCM's auditory processing of birdsong. Using immunocytochemistry, we show that approximately half of NCM's neurons are GABAergic. Whole cell patch-clamp recordings in a slice preparation demonstrate that, at rest, spontaneously active GABAergic synapses inhibit excitatory inputs onto NCM neurons via GABA A receptors. Multi-electrode electrophysiological recordings in awake birds show that local blockade of GABA A-mediated inhibition in NCM markedly affects the temporal pattern of song-evoked responses in NCM without modifications in frequency tuning. Surprisingly, this blockade increases the phasic and largely suppresses the tonic response component, reflecting dynamic relationships of inhibitory networks that could include disinhibition. Thus processing of learned natural communication sounds in songbirds, and possibly other vocal learners, may depend on complex interactions of inhibitory networks.

Estradiol Shapes Auditory Processing in the Adult Brain by Regulating Inhibitory Transmission and Plasticity-Associated Gene Expression

“…All procedures described below were approved by the University Committee on Animal Resources of the University of Rochester. For neurophysiological recordings in awake, restrained birds, we used methodologies that we have described previously in detail (Pinaud et al, 2008c). Briefly, animals were anesthetized with Equithesin (combination of chloral hydrate at 200 mg/kg and sodium pentobarbital at 50 mg/kg, i.m.)…”

“…2 B, D,F ). This was accomplished by quantifying the difference between the mean absolute [the root-mean-squared (RMS)] value obtained for each electrode during a response window (from stimulus onset to stimulus offset plus 100 ms) and the mean absolute value during a control window (500 ms before stimulus onset) (Pinaud et al, 2008c). To compute these values either for control or stimulus windows, each digitized value is squared, the mean of these squares over the response interval is computed, and the square root of that mean is obtained.…”

“…This method provides a means of rectifying either single unit or multiunit neural activity for averaging across trials and calculating its average power (hence, we occasionally refer to results obtained with this method as the "rectified response amplitude" in the present work). The RMS approach is also highly useful to measure variability induced by drug application at each recording site, in the form of postdrug/predrug response amplitude ratios, as described above (a ratio of 1 indicates no drug-induced changes in response amplitude, whereas ratios Ͻ1 or Ͼ1 indicate decreases or increases in response amplitude, respectively), as detailed previously (Pinaud et al, 2008c).…”

“…Thus, along with discharge rate measurements, the RMS method provides a complementary approach for assessing drug-induced changes in neuronal physiology, thereby providing a more comprehensive description of the physiological changes in NCM responses (Chew et al, 1995(Chew et al, , 1996Pinaud et al, 2008c).…”

Glutamatergic circuits in the song system of Zebra Finch brain determined by gene expression of Vglut2 and Glutamate receptors

“…The descending motor pathway consisted of a set of nuclei including, dorsomedial nucleus of the intercollicular complex, retroambigual nucleus and tracheosyringeal motor nucleus of the hypoglossal nerve (Nottebohm et al, 1976;Wild, 1993). Pharmacological and electrophysiological studies investigating glutamatergic neurotransmission in the song system indicate that glutamate plays an important role for neuronal mechanisms of learning, memory, imprinting, or plasticity (Mooney and Konishi, 1991;Basham et al, 1999;Pinaud et al, 2008). However, glutamatergic circuits have not yet been characterized in thesong control nuclei of the songbird brain.…”