First order temporal properties of spontaneous and tone-evoked activity of auditory afferent neurones in the cochlear ganglion of the pigeon.
Spontaneous and tone-evoked single-unit activity was recorded from afferent neurones in the cochlear ganglion of the anaesthetized pigeon, and the data analysed in a way that allowed the physics of underlying mechanisms to be described. The periodicity of neural activity was quantified by Fourier analysis of the histogram of successive spike intervals. Spontaneous activity was quasiperiodic for 57% of neurones (average rate: 74 s-1); it was irregular for the remainder of neurones (average rate: 55 s-1). The preferred frequency (PF) of the quasiperiodic spontaneous activity was, on average, equal to the characteristic frequency (CF) of the neurone (70% of cases) or CF/2 (30%). This observation can be explained by supposing that preferred intervals of spontaneous activity are generated by noise passing through a filter tuned to the CF of the neurone; in most cases (70%) discharge was synchronized to CF, but in the others the neurone fired to every second cycle of the filtered signal. Consistent with this interpretation, for 79% of neurones, the modal interval of spontaneous activity was, on average, directly proportional to the CF-period, irrespective of whether preferred intervals were detected. The synchronization index at the PF was inversely related to the PF, and was quantified by the amplitude response of a first-order low-pass filter with cutoff frequency of 48 +/- 18 Hz. The spontaneous activity of 9% of neurones exhibited a second-harmonic component of the PF. For both tone-evoked and spontaneous activity, the observed synchronization indices of harmonics of the stimulus frequency or of the PF were consistent with an underlying exponential spike-generator function. If such a function does indeed govern spike generation, then it implies that the Shannon entropy of the probability density function of the instantaneous firing rate is near its maximum value and suggests that the system is close to statistical equilibrium. Single-tone rate-suppression was detected for 53% of those neurones that exhibited multiple preferred intervals of spontaneous activity. It is conjectured that the phenomena of quasiperiodic spontaneous activity and single-tone rate-suppression are different aspects of a single presynaptic process. According to this model, we would expect to find these two phenomena in animals that have auditory fibres innervating electrically tuned hair cells, and that have stereocilia firmly coupled to a tectorial membrane.
Gummer
A W
AW
Australian National University, Research School of Biological Sciences, Developmental Neurobiology Group, Canberra, Australia.
D000161:Acoustic Stimulation; D000200:Action Potentials; D000344:Afferent Pathways / Q000502:physiology; D000818:Animals; D001306:Auditory Pathways / Q000502:physiology; D010856:Columbidae; D005072:Evoked Potentials, Auditory; D005583:Fourier Analysis; D008959:Models, Neurological; D009474:Neurons / Q000502:physiology; D013045:Species Specificity; D013136:Spiral Ganglion / Q000502:physiology*; D000159:Vestibulocochlear Nerve / Q000502:physiology*