Multi-dimensional tuning in motor cortical neurons during active behavior

Abstract

A region within songbird cortex, AId (dorsal intermediate arcopallium), is functionally analogous to motor cortex in mammals and has been implicated in vocal learning during development. AId thus serves as a powerful model for investigating motor cortical contributions to developmental skill learning. We made extracellular recordings in AId of freely behaving juvenile zebra finches and evaluated neural activity during diverse motor behaviors throughout entire recording sessions, including song production as well as hopping, pecking, preening, fluffups, beak interactions with cage objects, scratching, and stretching. A large population of single neurons showed significant modulation of activity during singing relative to quiescence. In addition, AId neurons demonstrated heterogeneous response patterns that were evoked during multiple movements, with single neurons often demonstrating excitation during one movement type and suppression during another. Lesions of AId do not disrupt vocal motor output or impair generic movements, suggesting that the responses observed during active behavior do not reflect direct motor drive. Consistent with this idea, we found that some AId neurons showed differential activity during pecking movements depending on the context in which pecks occurred, suggesting that AId circuitry encodes diverse inputs beyond generic motor parameters.Moreover, we found evidence of neurons that did not respond during discrete movements but were nonetheless modulated during active behavioral states compared to quiescence. Taken together, our results support the idea that AId neurons are involved in sensorimotor integration of external sensory inputs and/or internal feedback cues to help modulate goal-directed behaviors. SIGNIFICANCE STATEMENTMotor cortex across taxa receives highly integrated, multi-modal information and has been implicated in both execution and acquisition of complex motor skills, yet studies of motor cortex typically employ restricted behavioral paradigms that target select movement parameters, preventing wider assessment of the diverse sensorimotor factors that can affect motor cortical activity. Recording in AId of freely behaving juvenile songbirds that are actively engaged in sensorimotor learning offers unique advantages for elucidating the functional role of motor cortical neurons. The results demonstrate that a diverse array of factors modulate motor cortical activity and lay important groundwork for future investigations of how multi-modal information is integrated in motor cortical regions to contribute to learning and execution of complex motor skills.3

Molecular specializations of deep cortical layer analogs in songbirds

“…The RA is considered part of the intermediate arcopallium, which is the major source of descending output from the avian telencephalon 38 . The arcopallium, more broadly, is thought to contain the avian analog of the deep layers of the mammalian sensory and motor cortices based on similarities in their projection patterns 31 , 39 , neuronal activation 33 , 40 , and transcriptional profiles 41 – 44 , but may also contain the avian equivalent of pallial parts of the mammalian amygdala 44 – 46 . Avian analogs of RA are found in other birds that evolved vocal learning 9 – 13 , but are thought to be absent in vocal non-learning birds based on cytoarchitectonics and molecular criteria 14 – 16 , 47 ; but see also 17 , 18 .…”

“…For RA, there is evidence of severe vocal deficits after lesioning 5 and evidence of activation during singing based on electrophysiological recordings 36 , 37 and immediate early gene expression 52 . Although less studied, evidence for a motor control function for AId comes from the immediate early gene activation during movements such as wing flapping, hopping, and pecking 33 , 40 , and the severe motor deficits associated with large lesions 53 . Interestingly, the age differences we observed in gene expression suggest that AId undergoes molecular changes during development, which could be associated with vocal or other motor learning refinement.…”

“…Other studies suggest common motor control functions of RA and AId. For example, AId shows immediate early gene expression after movements such as wing flapping or hopping 33 , 40 , analogous to RA being active during song production 35 , 36 , 52 . Furthermore, while lesions to RA result in severe song deficits 5 , birds show marked motor deficits including akinesia and immobility in large lesions that primarily include AId 53 .…”

Movement signaling in ventral pallidum and dopaminergic midbrain is gated by behavioral state in singing birds

“…Instead, we have measured acceleration at the level of the head, and computed onset and offset timing of movements. While birds appear to move in similar ways during singing and non-singing periods (Yuan and Bottjer 2020), it’s possible that there are subtle systematic differences between ostensibly similar movements when performed during singing and non-singing. Future work with high speed video will be required to test this possibility.…”