Local field potentials in a pre-motor region predict learned vocal sequences

Abstract

Neuronal activity within the premotor region HVC is tightly synchronized to, and crucial for, the articulate production of learned song in birds. Characterizations of this neural activity detail patterns of sequential bursting in small, carefully identified subsets of neurons in the HVC population. The dynamics of HVC are well described by these characterizations, but have not been verified beyond this scale of measurement. There is a rich history of using local field potentials (LFP) to extract information about behavior that extends beyond the contribution of individual cells. These signals have the advantage of being stable over longer periods of time, and they have been used to study and decode human speech and other complex motor behaviors. Here we characterize LFP signals presumptively from the HVC of freely behaving male zebra finches during song production to determine if population activity may yield similar insights into the mechanisms underlying complex motor-vocal behavior. Following an initial observation that structured changes in the LFP were distinct to all vocalizations during song, we show that it is possible to extract time-varying features from multiple frequency bands to decode the identity of specific vocalization elements (syllables) and to predict their temporal onsets within the motif. This demonstrates the utility of LFP for studying vocal behavior in songbirds. Surprisingly, the time frequency structure of HVC LFP is qualitatively similar to well-established oscillations found in both human and non-human mammalian motor areas. This physiological similarity, despite distinct anatomical structures, may give insight into common computational principles for learning and/or generating complex motor-vocal behaviors.

Oscillations without cortex: Working memory modulates brainwaves in the endbrain of crows

“…Therefore, our results indicate that the assumption that a (cortical) layering of dendrites is required for oscillations, is not valid. This is in line with recent other observations of modulated gamma in the (non-layered) telencephalon of birds: in the song system of singing zebra finches ( Brown et al, 2021 , Lewandowski and Schmidt, 2011 ) and in the hippocampus of sleeping zebra finches ( van der Meij et al, 2020 ). Our results now show that such gamma oscillations occur in a modulated fashion during ongoing higher cognitive functions like working memory.…”

“…Most prominently, the optic tectum and neighboring tegmental nuclei show modulation in the gamma range during attention ( Goddard et al, 2012 , Neuenschwander and Varela, 1993 , Sridharan et al, 2011 , Sridharan and Knudsen, 2015 ). Gamma band modulations were further reported in the avian forebrain during birdsong ( Brown et al, 2021 , Lewandowski and Schmidt, 2011 , Spool et al, 2021 ), and in the avian hippocampal formation in vitro ( Dheerendra et al, 2018 ) and during sleep ( van der Meij et al, 2020 ). However, these observations cannot answer the question of whether oscillations underlie higher cognition since they were either made in the neatly layered optic tectum, were tightly linked to motor behavior, or occurred in sleeping birds.…”

Analogies of human speech and bird song: From vocal learning behavior to its neural basis

“…The observation of local field potential (LFP) signals in male zebra finches during singing indicates that the characteristic changes of time frequency structure of HVC LFP may correspond to specific syllables in the motif song. In addition, the HVC LFP signal features are similar to those LFP signals associated with motor control in mammals, including humans and non-human primates (Brown et al, 2021). Language-related premotor neural activity was found early in the human Broca's area by electrophysiological recordings (Fried et al, 1981;Jarvis, 2004), while this area also receives signal input from the temporal auditory cortex and transmits the integrated auditory information to LMC and ASt, respectively (Doupe and Kuhl, 1999;Bolhuis and Gahr, 2006;Bolhuis et al, 2010).…”

Oscillations without cortex: Working memory modulates brainwaves in the endbrain of crows

“…Only recently modulated gamma was reported in the (non-layered) telencephalon of birds. In the song system of singing zebra finches (Brown et al, 2021; Lewandowski & Schmidt, 2011), and in the hippocampus of sleeping zebra finches (van der Meij et al, 2020). Functionally involved in such gamma oscillations are excitatory cell types, homologous to mammalian excitatory neurons, which are part of neuronal circuitry that can be optogenetically induced to produce broad range gamma oscillations (Spool et al, 2021), Fig.…”

“…Most prominently the optic tectum and neighboring tegmental nuclei show modulation in the gamma range during attention (Goddard et al, 2012; Neuenschwander & Varela, 1993; Sridharan et al, 2011; Sridharan & Knudsen, 2015). Gamma band modulations were further reported in the avian forebrain during birdsong (Brown et al, 2021; Lewandowski & Schmidt, 2011; Spool et al, 2021), and in the avian hippocampal formation in vitro (Dheerendra et al, 2018) and during sleep (van der Meij et al, 2020). However, these observations cannot answer the question of whether oscillations underlie higher cognition since they were either made in the neatly layered optic tectum, were tightly linked to motor behavior, or occurred in sleeping birds.…”