Abstract
A question central to sensory processing is how signal information is encoded and processed by single neurons. Stimulus features can be represented through rate coding (via firing rate), temporal coding (via firing synchronization to temporal periodicities), or temporal encoding (via intricate patterns of spike trains). Of the three, examples of temporal encoding are the least documented. One region in which temporal encoding is currently being explored is the auditory midbrain. Midbrain neurons in the plainfin midshipman generate different interspike interval (ISI) distributions depending on the frequencies of the concurrent vocal signals. However, these distributions differ only along certain lengths of ISIs, so that any neurons trying to distinguish the distributions would have to respond selectively to specific ISI ranges. We used this empirical observation as a realistic challenge with which to explore the plausibility of ISI-tuned neurons that could validate this form of temporal encoding. The resulting modeled cells—point neurons optimized through multidimensional searching—were successfully tuned to discriminate patterns in specific ranges of ISIs. Achieving this task, particularly with simplified neurons, strengthens the credibility of ISI coding in the brain and lends credence to its role in auditory processing.
Similar content being viewed by others
References
Balis UJ, Morris KF, Koleski J, Lindsey BG (1994) Simulations of a ventrolateral medullary neural network for respiratory rhythmogenesis inferred from spike train cross-correlation. Biol. Cybern. 70:311-327.
Bass AH, Bodnar DA, Marchterre MA (2000) Midbrain acoustic circuitry in a vocalizing fish. J. Comp. Neur. 419:505-531.
Bodnar DA, Bass AH (1997) Temporal coding of concurrent acoustic signals in auditory midbrain. J. Neurosci. 17:7553-7564.
Bodnar DA, Bass AH (1999) Midbrain combinatorial code for temporal and spectral information in concurrent acoustic signals. J. Neurophys. 81:213-232.
Brantely RK, Bass AH (1994) Alternative male spawning tactics and acoustic signals in the plainfin midshipman, Porichthys notatus. Ethology 96:213-232.
Buonomano DV (2000) Decoding temporal information: A model based on short-term synaptic plasticity. J. Neurosci. 20:1129-1141.
Cariani P, Delgutte B (1996) Neural correlates of the pitch of complex tones. I. Pitch and pitch salience. J. Neurophysiol. 76:1698-1716.
Fay RR (1993) Structure and function in sound discrimination among vertebrates. In: Webster DB, ed. The Evolutionary Biology of Herring. Springer, New York. pp. 229-266.
Fay RR (1995) Perception of spectrally and temporally complex sounds by the goldfish (Carassius auratus). Hear. Res. 89:146-154.
Ghazanfar AA, Stambaugh CR, Nicolelis MAL (2000) Encoding of tactile stimulus location by somatosensory thalamocortical ensembles. J. Neurosci. 20:3761-3775.
Ghoshal S, Kim DO, Northrop RB (1992) Amplitude-modulated tone encoding behavior of cochlear nucleus neurons: Modeling study. Hear. Res. 58:153-165.
Hill, AV (1936) Excitation and accommodation in nerve. Proc. R. Soc. London, Ser. B. 119:305-355.
Ibara RM, Penny LT, Ebeling AW, van Dykhuizen G, Cailliet G (1983) The mating call of the plainfin midshipman fish, Porichthys notatus. In: DGL Noakes, DG Lindquist, GS Helfman, JA Ward, eds. Predators and Prey in Fish. Junk Press, The Hague, Netherlands.
Jack JJ, Noble D, Tsien RW (1975) Electrical Current Flow in Excitable Cells. Clarendon Press, Oxford.
Keilson SE, Richards VM, Wyman BT, Young ED (1997) The representation of concurrent vowels in the cat anesthetized ventral cochlear nucleus: Evidence for a periodicity-tagged spectral representation. J. Acoust. Soc. Am. 102:1056-1071.
Kernell D (1968) The repetitive impulse discharge of a simple neuron model compared to that of spiral motoneurons. Brain Res. 11:685-687.
Kirkpatrick S, Gelatt CD, Vecchi MP (1983) Optimization by simulated annealing. Science 220:671-680.
Laurent G, Wehr M, Davidowitz H (1996) Temporal representations of odors in an olfactory network. J. Neurosci. 16:3837-3847.
Licklider JCR (1951) A duplex theory of pitch perception. Experientia. 7:128-134.
Licklider JCR (1956) Auditory frequency analysis. In: Cherry C, ed. Information Theory, Third London Symposium. Butterworths Scientific Publications, London. pp. 253-268.
MacGregor RJ (1987) Neural and Brain Modeling. Academic Press, San Diego.
MacGregor RJ, Oliver RM (1974) A model for repetitive firing in neurons. Biol. Cybernet. 40:113-126.
McClurkin JW, Optican LM, Richmond BJ, Gawne TJ (1991) Concurrent processing and complexity of temporally encoded neuronal messages in visual perception. Science 253:675-677.
McKibben JR, Bass AH (1998) Behavioral assessment of acoustic parameters relevant to signal recognition and preference in a vocal fish. J. Acoust. Soc. Am. 104:3520-3533.
McKibben JR, Bass AH (1999) Peripheral encoding of behaviorally relevant acoustic signals in a vocal fish: Signal tones. J. Comp. Physiol. A. 184:563-576.
McKibben JR, Bass AH (in review) Peripheral encoding of behaviorally relevant acoustic signals in a vocal fish: harmonic and beat stimuli. J. Comp. Physiol.
Merzenich MM, Reid MD (1974) Representation of the cochlea within the inferior colliculus of the cat. Brain Res. 77:397-415.
Middlebrooks JC, Clock AE, Xu L, Green DM (1994) A panoramic code for sound location by cortical neurons. Science 264:842-844.
Nelder JA, Mead R (1965) A simplex method for function minimization. Computer J. 8:308-313.
Palmer AR (1990) The representation of the spectra and fundamental frequency of steady-state single-and double-vowel sounds in the temporal discharge patterns of guinea pig cochlear nerve fibers. J. Acoust. Soc. Am. 88:1412-1426.
Popper AN, Fay RR (1993) Sound detection and processing by fish: Critical review and major research questions. Brain Behav. Evol. 41:14-38.
Reich DS, Mechler F, Purpura KP, Victor JD (2000) Inter-spike intervals, receptive fields, and information encoding in primary visual cortex. J. Neurosci. 20:1964-1974.
Rees A, Sarbaz A, Malimerica MS, LeBeau FEN (1997) Regularity of firing of neurons in the inferior colliculus. J. Neurophysiol. 77:2945-2965.
Richmond BJ, Optican LM, Spitzer H (1990) Temporal encoding of two-dimensional patterns by single units in primate visual cortex. I Stimulus-response relations. J. Neurophysiol. 64:351-368.
Schreiner CE, Langner G (1994) Laminar structure of frequency organization in auditory midbrain. Nature 388:383-386.
Semple MN, Aitkin LM (1979) Representation of sound frequency and laterality by units in the central nucleus of cat inferior colliculus. J. Neurophsiol. 42:1626-1639.
Theunissen F, Miller JP (1995) Temporal encoding in the nervous system: A rigorous definition. J. Comput. Neurosci. 2:149-162.
Wehr M, Laurent G (1996) Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384: 162-166.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wilson, N.R., Bodnar, D.A., Skovira, J.F. et al. Processing of Auditory Midbrain Interspike Intervals by Model Neurons. J Comput Neurosci 10, 151–172 (2001). https://doi.org/10.1023/A:1011217030303
Issue Date:
DOI: https://doi.org/10.1023/A:1011217030303