Temperature Manipulation in Songbird Brain Implicates the Premotor Nucleus HVC in Birdsong Syntax.
Variable motor sequences of animals are often structured and can be described by probabilistic transition rules between action elements. Examples include the songs of many songbird species such as the Bengalese finch, which consist of stereotypical syllables sequenced according to probabilistic rules (song syntax). The neural mechanisms behind such rules are poorly understood. Here, we investigate where the song syntax is encoded in the brain of the Bengalese finch by rapidly and reversibly manipulating the temperature in the song production pathway. Cooling the premotor nucleus HVC (proper name) slows down the song tempo, consistent with the idea that HVC controls moment-to-moment timings of acoustic features in the syllables. More importantly, cooling HVC alters the transition probabilities between syllables. Cooling HVC reduces the number of repetitions of long-repeated syllables and increases the randomness of syllable sequences. In contrast, cooling the downstream motor area RA (robust nucleus of the acropallium), which is critical for singing, does not affect the song syntax. Unilateral cooling of HVC shows that control of syllables is mostly lateralized to the left HVC, whereas transition probabilities between the syllables can be affected by cooling HVC in either hemisphere to varying degrees. These results show that HVC is a key site for encoding song syntax in the Bengalese finch. HVC is thus involved both in encoding timings within syllables and in sequencing probabilistic transitions between syllables. Our finding suggests that probabilistic selections and fine-grained timings of action elements can be integrated within the same neural circuits.SIGNIFICANCE STATEMENTMany animal behaviors such as birdsong consist of variable sequences of discrete actions. Where and how the probabilistic rules of such sequences are encoded in the brain is poorly understood. We locally and reversibly cooled brain areas in songbirds during singing. Mild cooling of area HVC in the Bengalese finch brain-a premotor area homologous to the mammalian premotor cortex-alters the statistics of the syllable sequences, suggesting that HVC is critical for birdsong sequences. HVC is also known for controlling moment-to-moment timings within syllables. Our results show that timing and probabilistic sequencing of actions can share the same neural circuits in local brain areas.
Department of Physics.
Yisi S
YS
Zhang
Department of Physics.
Jason D
JD
Wittenbach
Department of Physics, dzj2@psu.edu.|Center for Neural Engineering, Pennsylvania State University, University Park, Pennsylvania 16802.
Dezhe Z
0000-0003-4401-0713
DZ
Jin
Department of Physics.|Department of Psychology, and.
Alexay A
AA
Kozhevnikov
D000222:Adaptation, Physiological / Q000502:physiology*; D000818:Animals; D001833:Body Temperature Regulation / Q000502:physiology*; D004525:Efferent Pathways / Q000502:physiology; D046369:Finches / Q000502:physiology*; D008297:Male; D009044:Motor Cortex / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*; D012660:Semantics; D014828:Vocalization, Animal / Q000502:physiology*
Bengalese finch; HVC; birdsong; birdsong syntax; cooling; lateralization