Abstract
The brain must solve a wide range of different temporal problems, each of which can be defined by a relevant time scale and specific functional requirements. Experimental and theoretical studies suggest that some forms of timing reflect general and inherent properties of local neural networks. Like the ripples on a pond, neural networks represent rich dynamical systems that can produce time-varying patterns of activity in response to a stimulus. State-dependent network models propose that sensory timing arises from the interaction between incoming stimuli and the internal dynamics of recurrent neural circuits. A wide-variety of time-dependent neural properties, such as short-term synaptic plasticity, are important contributors to the internal dynamics of neural circuits. In contrast to sensory timing, motor timing requires that network actively generate appropriately timed spikes even in the absence of sensory stimuli. Population clock models propose that motor timing arises from internal dynamics of recurrent network capable of self-perpetuating activity.
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References
Liberman AM, Delattre PC, Gerstman LJ, Cooper FS. Tempo of frequency change as a cue for distinguishing classes of speech sounds. J Exp Psychol. 1956;52:127–37.
Scott DR. Duration as a cue to the perception of a phrase boundary. J Acoust Soc Am. 1982;71(4):996–1007.
Schirmer A. Timing speech: a review of lesion and neuroimaging findings. Brain Res Cogn Brain Res. 2004;21(2):269–87.
Shannon RV, Zeng FG, Kamath V, Wygonski J, Ekelid M. Speech recognition with primarily temporal cues. Science. 1995;270(5234):303–4.
Breitenstein C, Van Lancker D, Daum I. The contribution of speech rate and pitch variation to the perception of vocal emotions in a German and an American sample. Cogn Emot. 2001;15(1):57–79.
Mauk MD, Buonomano DV. The neural basis of temporal processing. Annu Rev Neurosci. 2004;27:307–40.
Buonomano DV, Mauk MD. Neural network model of the cerebellum: temporal discrimination and the timing of motor responses. Neural Comput. 1994;6:38–55.
Mauk MD, Donegan NH. A model of Pavlovian eyelid conditioning based on the synaptic organization of the cerebellum. Learn Mem. 1997;3:130–58.
Medina JF, Mauk MD. Computer simulation of cerebellar information processing. Nat Neurosci. 2000;3(Suppl):1205–11.
Herculano-Houzel S. The human brain in numbers: a linearly scaled-up primate brain. Front Hum Neurosci. 2009;3:32 (Original Research Article).
Broome BM, Jayaraman V, Laurent G. Encoding and decoding of overlapping odor sequences. Neuron. 2006;51(4):467–82.
Engineer CT, Perez CA, Chen YH, Carraway RS, Reed AC, Shetake JA, et al. Cortical activity patterns predict speech discrimination ability. Nat Neurosci. 2008;11:603–8.
Churchland MM, Yu BM, Sahani M, Shenoy KV. Techniques for extracting single-trial activity patterns from large-scale neural recordings. Curr Opin Neurobiol. 2007;17(5):609–18.
Schnupp JW, Hall TM, Kokelaar RF, Ahmed B. Plasticity of temporal pattern codes for vocalization stimuli in primary auditory cortex. J Neurosci. 2006;26(18):4785–95.
Itskov V, Curto C, Pastalkova E, Buzsáki G. Cell assembly sequences arising from spike threshold adaptation keep track of time in the hippocampus. J Neurosci. 2011;31(8):2828–34.
Jin DZ, Fujii N, Graybiel AM. Neural representation of time in cortico-basal ganglia circuits. Proc Natl Acad Sci U S A. 2009;106(45):19156–61.
Lebedev MA, O’Doherty JE, Nicolelis MAL. Decoding of temporal intervals from cortical ensemble activity. J Neurophysiol. 2008;99(1):166–86.
Crowe DA, Averbeck BB, Chafee MV. Rapid sequences of population activity patterns dynamically encode task-critical spatial information in parietal cortex. J Neurosci. 2010;30(35):11640–53.
Hahnloser RHR, Kozhevnikov AA, Fee MS. An ultra-sparse code underlies the generation of neural sequence in a songbird. Nature. 2002;419:65–70.
Long MA, Jin DZ, Fee MS. Support for a synaptic chain model of neuronal sequence generation. Nature. 2010;468(7322):394–9. doi:10.1038/nature09514.
Zucker RS. Short-term synaptic plasticity. Annu Rev Neurosci. 1989;12:13–31.
Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol. 2002;64:355–405.
Newberry NR, Nicoll RA. A bicuculline-resistant inhibitory post-synaptic potential in rat hippocampal pyramidal cells in vitro. J Physiol. 1984;348(1):239–54.
Buonomano DV, Merzenich MM. Net interaction between different forms of short-term synaptic plasticity and slow-IPSPs in the hippocampus and auditory cortex. J Neurophysiol. 1998;80:1765–74.
Batchelor AM, Madge DJ, Garthwaite J. Synaptic activation of metabotropic glutamate receptors in the parallel fibre-Purkinje cell pathway in rat cerebellar slices. Neuroscience. 1994;63(4):911–5.
Johnston D, Wu SM. Foundations of cellular neurophysiology. Cambridge: MIT Press; 1995.
Hooper SL, Buchman E, Hobbs KH. A computational role for slow conductances: single-neuron models that measure duration. Nat Neurosci. 2002;5:551–6.
Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003;4(7):517–29.
Burnashev N, Rozov A. Presynaptic Ca2+ dynamics, Ca2+ buffers and synaptic efficacy. Cell Calcium. 2005;37(5):489–95.
Lester RAJ, Clements JD, Westbrook GL, Jahr CE. Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature. 1990;346(6284):565–7.
Reyes A, Sakmann B. Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J Neurosci. 1999;19:3827–35.
Markram H, Wang Y, Tsodyks M. Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci U S A. 1998;95:5323–8.
Dobrunz LE, Stevens CF. Response of hippocampal synapses to natural stimulation patterns. Neuron. 1999;22(1):157–66.
Fukuda A, Mody I, Prince DA. Differential ontogenesis of presynaptic and postsynaptic GABAB inhibition in rat somatosensory cortex. J Neurophysiol. 1993;70(1):448–52.
Lambert NA, Wilson WA. Temporally distinct mechanisms of use-dependent depression at inhibitory synapses in the rat hippocampus in vitro. J Neurophysiol. 1994;72(1):121–30.
Ivry RB, Schlerf JE. Dedicated and intrinsic models of time perception. Trends Cogn Sci. 2008;12(7):273–80.
Buonomano DV, Merzenich MM. Temporal information transformed into a spatial code by a neural network with realistic properties. Science. 1995;267:1028–30.
Lee TP, Buonomano DV. Unsupervised formation of vocalization-sensitive neurons: a cortical model based on short-term and homeostatic plasticity. Neural Comput. 2012;24:2579–603.
Buonomano DV. Decoding temporal information: a model based on short-term synaptic plasticity. J Neurosci. 2000;20:1129–41.
Maass W, Natschläger T, Markram H. Real-time computing without stable states: a new framework for neural computation based on perturbations. Neural Comput. 2002;14:2531–60.
Maass W, Natschläger T, Markram H. A model of real-time computation in generic neural microcircuits. Adv Neural Inf Process Syst. 2003;15:229–36.
Haeusler S, Maass W. A Statistical analysis of information-processing properties of lamina-specific cortical microcircuit models. Cereb Cortex. 2007;17(1):149–62.
Karmarkar UR, Buonomano DV. Timing in the absence of clocks: encoding time in neural network states. Neuron. 2007;53(3):427–38.
Edwards CJ, Leary CJ, Rose GJ. Counting on inhibition and rate-dependent excitation in the auditory system. J Neurosci. 2007;27(49):13384–92.
Edwards CJ, Leary CJ, Rose GJ. Mechanisms of long-interval selectivity in midbrain auditory neurons: roles of excitation, inhibition, and plasticity. J Neurophysiol. 2008;100(6):3407–16.
Rose G, Leary C, Edwards C. Interval-counting neurons in the anuran auditory midbrain: factors underlying diversity of interval tuning. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2011;197(1):97–108.
Carlson BA. Temporal-pattern recognition by single neurons in a sensory pathway devoted to social communication behavior. J Neurosci. 2009;29(30):9417–28.
Kostarakos K, Hedwig B. Calling song recognition in female crickets: temporal tuning of identified brain neurons matches behavior. J Neurosci. 2012;32(28):9601–12.
Shepherd GM. The synaptic organization of the brain. New York: Oxford University; 1998.
Carvalho TP, Buonomano DV. Differential effects of excitatory and inhibitory plasticity on synaptically driven neuronal input–output functions. Neuron. 2009;61(5):774–85.
Pouille F, Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science. 2001;293:1159–63.
Edwards CJ, Alder TB, Rose GJ. Auditory midbrain neurons that count. Nat Neurosci. 2002;5(10):934–6.
Alder TB, Rose GJ. Long-term temporal integration in the anuran auditory system. Nat Neurosci. 1998;1:519–23.
Sadagopan S, Wang X. Nonlinear spectrotemporal interactions underlying selectivity for complex sounds in auditory cortex. J Neurosci. 2009;29(36):11192–202.
Zhou X, de Villers-Sidani É, Panizzutti R, Merzenich MM. Successive-signal biasing for a learned sound sequence. Proc Natl Acad Sci U S A. 2010;107(33):14839–44.
Brosch M, Schreiner CE. Sequence sensitivity of neurons in cat primary auditory cortex. Cereb Cortex. 2000;10(12):1155–67.
Keele SW, Pokorny RA, Corcos DM, Ivry R. Do perception and motor production share common timing mechanisms: a correctional analysis. Acta Psychol (Amst). 1985;60(2–3):173–91.
Ivry RB, Hazeltine RE. Perception and production of temporal intervals across a range of durations – evidence for a common timing mechanism. J Exp Psychol Hum Percept Perform. 1995;21(1):3–18 [Article].
Perrett SP, Ruiz BP, Mauk MD. Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci. 1993;13:1708–18.
Raymond J, Lisberger SG, Mauk MD. The cerebellum: a neuronal learning machine? Science. 1996;272:1126–32.
Laje R, Cheng K, Buonomano DV. Learning of temporal motor patterns: an analysis of continuous vs. reset timing. Front Integr Neurosci. 2011;5:61 (Original Research).
Buonomano DV, Laje R. Population clocks: motor timing with neural dynamics. Trends Cogn Sci. 2010;14(12):520–7.
Buonomano DV, Karmarkar UR. How do we tell time? Neuroscientist. 2002;8(1):42–51.
Medina JF, Garcia KS, Nores WL, Taylor NM, Mauk MD. Timing mechanisms in the cerebellum: testing predictions of a large-scale computer simulation. J Neurosci. 2000;20(14):5516–25.
Yamazaki T, Tanaka S. The cerebellum as a liquid state machine. Neural Netw. 2007;20(3):290–7.
Ivry RB, Keele SW. Timing functions of the cerebellum. J Cogn Neurosci. 1989;1:136–52.
Sussillo D, Toyoizumi T, Maass W. Self-tuning of neural circuits through short-term synaptic plasticity. J Neurophysiol. 2007;97(6):4079–95.
Jaeger H, Haas H. Harnessing nonlinearity: predicting chaotic systems and saving energy in wireless communication. Science. 2004;304(5667):78–80.
Sussillo D, Abbott LF. Generating coherent patterns of activity from chaotic neural networks. Neuron. 2009;63(4):544–57.
Pastalkova E, Itskov V, Amarasingham A, Buzsaki G. Internally generated cell assembly sequences in the rat hippocampus. Science. 2008;321(5894):1322–7.
Buonomano DV. Timing of neural responses in cortical organotypic slices. Proc Natl Acad Sci U S A. 2003;100:4897–902.
Johnson HA, Goel A, Buonomano DV. Neural dynamics of in vitro cortical networks reflects experienced temporal patterns. Nat Neurosci. 2010;13(8):917–9. doi:10.1038/nn.2579.
Buonomano DV, Maass W. State-dependent Computations: Spatiotemporal Processing in Cortical Networks. Nat Rev Neurosci. 2009;10:113–125.
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Buonomano, D.V. (2014). Neural Dynamics Based Timing in the Subsecond to Seconds Range. In: Merchant, H., de Lafuente, V. (eds) Neurobiology of Interval Timing. Advances in Experimental Medicine and Biology, vol 829. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1782-2_6
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DOI: https://doi.org/10.1007/978-1-4939-1782-2_6
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