Manipulations of inhibition in cortical circuitry differentially affect spectral and temporal features of Bengalese finch song

The interplay between inhibition and excitation can regulate behavioral expression and control, including the expression of communicative behaviors like birdsong. Computational models postulate varying degrees to which inhibition within vocal motor circuitry influences birdsong, but few studies have tested these models by manipulating inhibition. Here we enhanced and attenuated inhibition in the cortical nucleus HVC (used as proper name) of Bengalese finches ( Lonchura striata var. domestica). Enhancement of inhibition (with muscimol) in HVC dose-dependently reduced the amount of song produced. Infusions of higher concentrations of muscimol caused some birds to produce spectrally degraded songs, whereas infusions of lower doses of muscimol led to the production of relatively normal (nondegraded) songs. However, the spectral and temporal structures of these nondegraded songs were significantly different from songs produced under control conditions. In particular, muscimol infusions decreased the frequency and amplitude of syllables, increased various measures of acoustic entropy, and increased the variability of syllable structure. Muscimol also increased sequence durations and the variability of syllable timing and syllable sequencing. Attenuation of inhibition (with bicuculline) in HVC led to changes to song distinct from and often opposite to enhancing inhibition. For example, in contrast to muscimol, bicuculline infusions increased syllable amplitude, frequency, and duration and decreased the variability of acoustic features. However, like muscimol, bicuculline increased the variability of syllable sequencing. These data highlight the importance of inhibition to the production of stereotyped vocalizations and demonstrate that changes to neural dynamics within cortical circuitry can differentially affect spectral and temporal features of song. NEW & NOTEWORTHY We reveal that manipulations of inhibition in the cortical nucleus HVC affect the structure, timing, and sequencing of syllables in Bengalese finch song. Enhancing and blocking inhibition led to opposite changes to the acoustic structure and timing of vocalizations, but both caused similar changes to vocal sequencing. These data provide support for computational models of song control but also motivate refinement of existing models to account for differential effects on syllable structure, timing, and sequencing.

Interhemispheric dominance switching in a neural network model for birdsong

Male zebra finches produce a sequence-invariant set of syllables, separated by short inspiratory gaps. These songs are learned from an adult tutor and maintained throughout life, making them a tractable model system for learned, sequentially ordered behaviors, particularly speech production. Moreover, much is known about the cortical, thalamic, and brain stem areas involved in producing this behavior, with the premotor cortical nucleus HVC (proper name) being of primary importance. In a previous study, our group developed a behavioral neural network model for birdsong constrained by the structural connectivity of the song system, the signaling properties of individual neurons and circuits, and circuit-breaking behavioral studies. Here we describe a more computationally tractable model and use it to explain the behavioral effects of unilateral cooling and electrical stimulations of HVC on song production. The model demonstrates that interhemispheric switching of song control is sufficient to explain these results, consistent with the hypotheses proposed when the experiments were initially conducted. Finally, we use the model to make testable predictions that can be used to validate the model framework and explain the effects of other perturbations of the song system, such as unilateral ablations of the primary input and output nuclei of HVC. NEW & NOTEWORTHY In this report, we propose a two-hemisphere neural network model for the bilaterally symmetrical song system underlying birdsong in the male zebra finch. This model captures the behavioral effects of unilateral cooling and electrical stimulations of the premotor cortical nucleus HVC during song production, supporting the hypothesis of interhemispheric switching of song control. We use the model to make testable predictions regarding the behavioral effects of other unilateral perturbations to the song system.

Neural activity in cortico-basal ganglia circuits of juvenile songbirds encodes performance during goal-directed learning

Cortico-basal ganglia circuits are thought to mediate goal-directed learning by a process of outcome evaluation to gradually select appropriate motor actions. We investigated spiking activity in core and shell subregions of the cortical nucleus LMAN during development as juvenile zebra finches are actively engaged in evaluating feedback of self-generated behavior in relation to their memorized tutor song (the goal). Spiking patterns of single neurons in both core and shell subregions during singing correlated with acoustic similarity to tutor syllables, suggesting a process of outcome evaluation. Both core and shell neurons encoded tutor similarity via either increases or decreases in firing rate, although only shell neurons showed a significant association at the population level. Tutor similarity predicted firing rates most strongly during early stages of learning, and shell but not core neurons showed decreases in response variability across development, suggesting that the activity of shell neurons reflects the progression of learning.

Regulation of vocal precision by local noradrenergic modulation of a motor nucleus

ABSTRACTRecent theories of norepinephrine (NE) function suggest that NE modulates the transition between stereotyped, goal-directed behavior and more variable exploratory behaviors that facilitate learning and adaptation. We provide evidence for context dependent switching by NE that is analogous to this explore/exploit strategy in the vocal system of the zebra finch (Taeniopygia guttata). Stimulation of the locus coeruleus, the major source of norepinephrine in the brain, decreases song trial-to-trial variability transforming the variable, exploratory “undirected” song into song that resembles the more stereotyped, exploitative “directed” song males sing to females. This behavioral switch is mediated by NE acting directly on a cortical motor nucleus that integrates inputs from a premotor cortical nucleus and a basal ganglia circuit necessary for vocal motor learning. These findings suggest that norepinephrine can act directly on the motor system to influence the transition between exploratory and exploitative behavioral strategies.

Amygdala in the regulation of reproductive functions during absence epilepsy

The monograph deals with the problems of general morphology of the amygdaloid body and for the first time the assessment of structural and functional changes in the anterior cortical nucleus of the amygdaloid body of the brain of WAG/Rij female rats (the recognized model of man’s absence epilepsy) in response to the modulating influence of sex hormones is made by means of a modern complex of research methods (electrophysiological, morphometric, histologic, immunohistochemical, submicroscopical and statistical ones). The changes in the electroencephalographic parameters of the anterior cortical nucleus, the reactive changes in neurons, glial anterior cortical nuclei of the amygdaloid body of the brain of WAG/Rij female rats at sex hormones deficiency and after the substitution therapy with 17β-estradiol in combination with progesterone are described in detail. The results of immunohistochemical analysis of astrocytic glia, of the analysis of synapsoarchitectonics and ultrastructural changes in neurons, glial cells, neuropil of the anterior cortical nucleus of the amygdaloid body of WAG / Rij rats at experimentally caused sex hormone deficiency and on the background of exogenous injection of 17β-estradiol in combination with progesterone into ovariectomized female rats are presented for the first time. The obtained new data on the morphofunctional features of the anterior cortical nucleus of the amygdaloid body of the brain significantly expand the notion of reactive changes in the anterior cortical nucleus at different levels of sex hormones and can be used by researchers of various profiles in studying this structure of the brain. The monograph is intended for neurobiologists of various specialities (neuromorphologists, neurophysiologists, neuroendocrinologists, neurochemists, etc.) engaged in the research of the amygdaloid body and the limbic system of the brain.

Cortical Processing of Odorants

Odorants, inhaled through the nose or exhaled from the mouth through the nose, bind to receptors on olfactory sensory neurons. Olfactory sensory neurons project in a highly stereotyped fashion into the forebrain to a structure called the olfactory bulb, where odorant-specific spatial patterns of neural activity are evoked. These patterns appear to reflect the molecular features of the inhaled stimulus. The olfactory bulb, in turn, projects to the olfactory cortex, which is composed of multiple sub-units including the anterior olfactory nucleus, the olfactory tubercle, the cortical nucleus of the amygdala, the anterior and posterior piriform cortex, and the lateral entorhinal cortex. Due to differences in olfactory bulb inputs, local circuitry and other factors, each of these cortical sub-regions appears to contribute to different aspects of the overall odor percept. For example, there appears to be some spatial organization of olfactory bulb inputs to the cortical nucleus of the amygdala, and this region may be involved in the expression of innate odor hedonic preferences. In contrast, the olfactory bulb projection to the piriform cortex is highly distributed and not spatially organized, allowing the piriform to function as a combinatorial, associative array, producing the emergence of experience-dependent odor-objects (e.g., strawberry) from the molecular features extracted in the periphery. Thus, the full perceptual experience of an odor requires involvement of a large, highly dynamic cortical network.

A distributed neural network model for the distinct roles of medial and lateral HVC in zebra finch song production

Zebra finch song consists of a string of syllables repeated in a nearly invariant sequence. We propose a neural network organization that can explain recent data indicating that the medial and lateral portions of the premotor cortical nucleus HVC have different roles in zebra finch song production. Our model explains these data, as well as data on the effects on song of cooling HVC, and makes predictions that we test in the singing bird.