A neural basis for auditory feedback control of vocal pitch.
Hearing one's own voice is essential for the production of correct vocalization patterns in many birds and mammals, including humans. Bats, for instance, adjust temporal, spectral, and intensity parameters of their echolocation calls by precisely monitoring the characteristics of the returning echo signals. However, neuronal substrates and mechanisms for auditory feedback control of vocalizations are still mostly unknown in any vertebrate. We used echolocating horseshoe bats to investigate the role of the midbrain and hindbrain tegmentum for the control of call frequencies in response to changing auditory feedback. These bats accurately control the frequency of their echolocation calls through auditory feedback both when the bat is at rest [resting frequency (RF)] and when it is flying and compensating for changes in echo frequency caused by flight-induced Doppler shifts [Doppler shift compensation (DSC)]. We iontophoretically injected various GABAergic and glutamatergic transmitter agonists and antagonists into the brainstem tegmentum. We found that within the parabrachial nuclei and the immediately adjacent tegmentum, excitatory effects caused by application of the glutamate agonist AMPA or the GABA(A) antagonist bicuculline raised RF and the frequency of calls emitted during DSC. Bicuculline application routinely blocked DSC altogether. Alternately, inhibitory effects caused by application of either the GABA(A) agonist muscimol or the AMPA antagonist CNQX lowered call frequencies emitted at rest and during DSC. Such an audio-vocal feedback mechanism might share basic aspects with audio-vocal feedback controlling the pitch of vocalizations in other mammals, including the involuntary response to "pitch-shifted feedback" in humans.
Smotherman
Michael
M
Department of Physiological Science, University of California, Los Angeles, Los Angeles, California 90095-1606, USA.
Zhang
Shuyi
S
Metzner
Walter
W
D018750:6-Cyano-7-nitroquinoxaline-2,3-dione / Q000494:pharmacology; D000818:Animals; D001640:Bicuculline / Q000494:pharmacology; D001931:Brain Mapping; D002685:Chiroptera; D004301:Doppler Effect; D004455:Echolocation; D018690:Excitatory Amino Acid Agonists / Q000494:pharmacology; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D025461:Feedback, Physiological; D018755:GABA Agonists / Q000494:pharmacology; D018756:GABA Antagonists / Q000494:pharmacology; D008636:Mesencephalon / Q000033:anatomy & histology / Q000187:drug effects / Q000502:physiology*; D010898:Pitch Perception; D012249:Rhombencephalon / Q000033:anatomy & histology / Q000187:drug effects / Q000502:physiology*; D014828:Vocalization, Animal; D018350:alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid / Q000494:pharmacology
D018690:Excitatory Amino Acid Agonists; D018691:Excitatory Amino Acid Antagonists; D018755:GABA Agonists; D018756:GABA Antagonists; D018750:6-Cyano-7-nitroquinoxaline-2,3-dione; D018350:alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid; D001640:Bicuculline