Processing of twitter-call fundamental frequencies in insula and auditory cortex of squirrel monkeys

Abstract Amplitude-modulated (AM) and frequency-modulated (FM) elements are prominent periodic sound features of squirrel monkeys’ twitter calls. To investigate how the periodic FM elements are represented in the spike activity of cortical neurons, single units in the insula, primary auditory field (AI) and rostral auditory field (R) were recorded. In five monkeys, 566 units (insula, n=181; AI, n=221; R, n=164) were exposed to synthesized fundamental frequencies and one natural twitter call. Neuronal encoding of periodic FM elements takes place by phase-locking to either the up- or the down-directed FM sweeps. The phase-locking was strongly influenced by the FM-period repetition rate. The ability of neurons in both auditory fields and the insula to encode all periodic FM elements showed a marked reduction at 16 Hz FM-period repetition rate. The neurons’ best frequency (BF) influenced the quality of periodicity encoding, but neurons with BFs outside the frequency range of the fundamentals also responded with periodic discharge rates. Even neurons in AI (6.8%) and the insula (22.6%) that did not respond to pure tones showed clear periodic FM encoding. The percentage of neurons able to encode all periodic FM elements within the twitter fundamental was significantly higher in field R than in AI and the insula. From 58 simultaneously recorded pairs of units in AI and the insula that had positive cross-correlation coefficients of spontaneous activity, the influence of the FM-period repetition rate on neuronal correlation was investigated. Correlated firing of AI and insula neurons seems limited to low-period repetition rates. The cross-correlation coefficients obtained for spontaneous activity and six different periodic FM sounds showed a band-pass characteristic. The natural twitter call evoked stronger neuronal responses in all fields than the synthesized fundamental frequencies with corresponding bi-directional FM sweeps. The better encoding of the transient features in the natural call can be attributed to the amplitude modulation added to the FM elements in the natural call. These amplitude modulations divide the FM elements of twitter calls into syllable-like sound elements. It is probable that encoding the complex pattern in the time and frequency domains of a call must undergo some integration at a cortical level. Additionally, these data provide the first evidence that insula neurons contribute to the encoding of complex FM signals.

[1]  M M Mesulam,et al.  Thalamic connections of the insula in the rhesus monkey and comments on the paralimbic connectivity of the medial pulvinar nucleus , 1984, The Journal of comparative neurology.

[2]  Brian C. J. Moore,et al.  Detection of combined frequency and amplitude modulation , 1992 .

[3]  M. Mesulam,et al.  The Insula of Reil in Man and Monkey , 1985 .

[4]  G. Salamon,et al.  Mutism and auditory agnosia due to bilateral insular damage—Role of the insula in human communication , 1995, Neuropsychologia.

[5]  J R Augustine,et al.  The insular lobe in primates including humans. , 1985, Neurological research.

[6]  J P Rauschecker,et al.  Processing of frequency-modulated sounds in the cat's posterior auditory field. , 1994, Journal of neurophysiology.

[7]  Hugo Fastl,et al.  Psychoacoustics: Facts and Models , 1990 .

[8]  H. Hopf,et al.  Localization of emotional and volitional facial paresis , 1992, Neurology.

[9]  J P Rauschecker,et al.  Processing of frequency-modulated sounds in the cat's anterior auditory field. , 1994, Journal of neurophysiology.

[10]  A Engelien,et al.  The functional anatomy of recovery from auditory agnosia. A PET study of sound categorization in a neurological patient and normal controls. , 1995, Brain : a journal of neurology.

[11]  R. Fifer.  Insular stroke causing unilateral auditory processing disorder: case report. , 1993, Journal of the American Academy of Audiology.

[12]  J. R. Augustine.  Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[13]  R. S. J. Frackowiak,et al.  Human cortical areas selectively activated by apparent sound movement , 1994, Current Biology.

[14]  H. Burton,et al.  The posterior thalamic region and its cortical projection in new world and old world monkeys , 1976, The Journal of comparative neurology.

[15]  H. Burton,et al.  Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular, parietal and temporal regions of primates , 1976, The Journal of comparative neurology.

[16]  D. N. Pandya,et al.  Insular interconnections with the amygdala in the rhesus monkey , 1981, Neuroscience.

[17]  J. Newman.  Squirrel Monkey Communication , 1985 .

[18]  A Reeves,et al.  Unit study of exteroceptive inputs to claustrocortex in awake, sitting, squirrel monkey. , 1971, Brain research.

[19]  J. Rauschecker,et al.  Processing of complex sounds in the macaque nonprimary auditory cortex. , 1995, Science.

[20]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[21]  B C Moore,et al.  Detection of combined frequency and amplitude modulation. , 1992, The Journal of the Acoustical Society of America.

[22]  J J Eggermont,et al.  Neural interaction in cat primary auditory cortex II. Effects of sound stimulation. , 1994, Journal of neurophysiology.

[23]  M. Mesulam,et al.  Insula of the old world monkey. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain , 1982, The Journal of comparative neurology.

[24]  Armin Bieser,et al.  AMPLITUDE ENVELOPE ENCODING AS A FEATURE FOR TEMPORAL INFORMATION PROCESSING IN THE AUDITORY CORTEX OF SQUIRREL MONKEYS , 1995 .