Differential developmental changes in cortical representations of auditory-vocal stimuli in songbirds

Abstract

Procedural skill learning requires iterative comparisons between feedback of self-generated motor output and a goal sensorimotor pattern. In juvenile songbirds, neural representations of both self-generated behaviors (each bird’s own immature song) and the goal motor pattern (each bird’s adult tutor song) are essential for vocal learning, yet little is known about how these behaviorally relevant stimuli are encoded. We made extracellular recordings during song playback in anesthetized juvenile and adult zebra finches ( Taeniopygia guttata) in adjacent cortical regions RA (robust nucleus of the arcopallium), AId (dorsal intermediate arcopallium), and RA cup, each of which is well situated to integrate auditory-vocal information: RA is a motor cortical region that drives vocal output, AId is an adjoining cortical region whose projections converge with basal ganglia loops for song learning in the dorsal thalamus, and RA cup surrounds RA and receives inputs from primary and secondary auditory cortex. We found strong developmental differences in neural selectivity within RA, but not in AId or RA cup. Juvenile RA neurons were broadly responsive to multiple songs but preferred juvenile over adult vocal sounds; in addition, spiking responses lacked consistent temporal patterning. By adulthood, RA neurons responded most strongly to each bird’s own song with precisely timed spiking activity. In contrast, we observed a complete lack of song responsivity in both juvenile and adult AId, even though this region receives song-responsive inputs. A surprisingly large proportion of sites in RA cup of both juveniles and adults did not respond to song playback, and responsive sites showed little evidence of song selectivity. NEW & NOTEWORTHY Motor skill learning entails changes in selectivity for behaviorally relevant stimuli across cortical regions, yet the neural representation of these stimuli remains understudied. We investigated how information important for vocal learning in zebra finches is represented in regions analogous to infragranular layers of motor and auditory cortices during vs. after the developmentally regulated learning period. The results provide insight into how neurons in higher level stages of cortical processing represent stimuli important for motor skill learning.

Multidimensional Tuning in Motor Cortical Neurons during Active Behavior

“…Gale et al, 2008). In addition, AIV clearly overlaps with or is identical to a region known as "RA cup," which is a putative auditory area that is located primarily ventral and anterior to RA (Kelley and Nottebohm, 1979;Vates et al, 1996;Mello et al, 1998;Yuan and Bottjer, 2019). We discuss the high degree of anatomical complexity in the arcopallial regions surrounding RA and AId in a Note to the paper by Mandelblat-Cerf et al…”

“…Such complex responses may result from multiple inputs relating to different movements or aspects of movements onto single AId neurons, as well as local transformation of afferent inputs. AId includes a local inhibitory network, evidenced by the fact that blocking GABA-A receptors in AId of anesthetized zebra finches elicits increased spontaneous firing rates, and parvalbumin expression is higher in AId compared to surrounding motor cortex (Mello et al, 2019;Yuan and Bottjer, 2019). Similarly, mammalian motor cortex contains a substantial population of inhibitory interneurons, which have been implicated in both regulating plasticity during motor skill learning and coordinating activity across motor cortex during behavior (Jacobs and Donoghue, 1991;Hess and Donoghue, 1994;Hess et al, 1996;Markram et al, 2004;Stagg et al, 2011;Donato et al, 2013;Chen et al, 2015;Kida et al, 2016;Adler et al, 2019).…”

Molecular specializations of deep cortical layer analogs in songbirds

“…AId has been hypothesized to be directly involved in vocal learning 54 . We note, though, that the adjacent ventral intermediate arcopallium (AIv) is an auditory area that responds to song playbacks 79 and may play a role in vocal learning 53 , 80 , thus the possible separate roles of these adjacent areas in auditory processing, vocal learning, and motor function remain to be conclusively determined.…”

Multi-dimensional tuning in motor cortical neurons during active behavior

“…We found that most AId neurons were selective for single movements or for different AId of anesthetized zebra finches elicits increased spontaneous firing rates, and parvalbumin expression is higher in AId compared to surrounding motor cortex (Mello et al, 2019;Yuan and Bottjer, 2019). Similarly, mammalian motor cortex contains a substantial population of inhibitory interneurons, which have been implicated in both regulating plasticity during motor skill learning and coordinating activity across motor cortex during behavior (Jacobs and Donoghue, 1991;Hess and Donoghue, 1994;Hess et al, 1996;Markram et al, 2004;Stagg et al, 2011;Donato et al, 2013;Chen et al, 2015;Kida et al, 2016;Adler et al, 2019).…”

“…Given convergent input from a diverse array of multi-modal processing streams, the tuning profiles of neurons in both avian and mammalian motor cortex often include not only motor but also sensory responsivity. For instance, neurons in RA, which lies adjacent to AId in songbird motor cortex, drive vocal motor output in singing birds and demonstrate robust responses to playback of song stimuli in anesthetized birds (Nottebohm et al, 1976;Doupe and Konishi, 1991;Vicario and Yohay, 1993;Wild, 1993;Yu and Margoliash, 1996;Dave et al, 1998;Dave and Margoliash, 2000;Leonardo and Fee, 2005;Kojima and Doupe, 2007;Sober et al, 2008;Yuan and Bottjer, 2019). Recordings from macaque motor cortex have likewise demonstrated sensitivity to non-motor stimuli: for instance, in visually-guided target-reaching paradigms, some motor cortical neurons exhibit selective activity related to the visual target, regardless of the limb trajectory used to reach that target (Tanji and Evarts, 1976;Evarts and Fromm, 1977;Murata et al, 1997;Shen and Alexander, 1997).…”