Mode-Locked Spike Trains in Responses of Ventral Cochlear Nucleus Chopper and Onset Neurons to Periodic Stimuli

Jonathan Laudanski, Stephen Coombes, Alan R. Palmer, Christian J. Sumner
2010 Journal of Neurophysiology  
Laudanski J, Coombes S, Palmer AR, Sumner CJ. Mode-locked spike trains in responses of ventral cochlear nucleus chopper and onset neurons to periodic stimuli. We report evidence of mode-locking to the envelope of a periodic stimulus in chopper units of the ventral cochlear nucleus (VCN). Mode-locking is a generalized description of how responses in periodically forced nonlinear systems can be closely linked to the input envelope, while showing temporal patterns of higher order than seen during
more » ... ure phase-locking. Re-analyzing a previously unpublished dataset in response to amplitude modulated tones, we find that of 55% of cells (6/11) demonstrated stochastic mode-locking in response to sinusoidally amplitude modulated (SAM) pure tones at 50% modulation depth. At 100% modulation depth SAM, most units (3/4) showed mode-locking. We use interspike interval (ISI) scattergrams to unravel the temporal structure present in chopper mode-locked responses. These responses compared well to a leaky integrate-and-fire model (LIF) model of chopper units. Thus the timing of spikes in chopper unit responses to periodic stimuli can be understood in terms of the complex dynamics of periodically forced nonlinear systems. A larger set of onset (33) and chopper units (24) of the VCN also shows mode-locked responses to steady-state vowels and cosine-phase harmonic complexes. However, while 80% of chopper responses to complex stimuli meet our criterion for the presence of mode-locking, only 40% of onset cells show similar complex-modes of spike patterns. We found a correlation between a unit's regularity and its tendency to display mode-locked spike trains as well as a correlation in the number of spikes per cycle and the presence of complex-modes of spike patterns. These spiking patterns are sensitive to the envelope as well as the fundamental frequency of complex sounds, suggesting that complex cell dynamics may play a role in encoding periodic stimuli and envelopes in the VCN. I N T R O D U C T I O N Spike timing is thought to play an important role in the neural representation of sound. It has long been studied in the context of phase-locking, in which a neuron tends to fire at a given phase of a periodic stimulus. This effect is robust in the auditory nerve (AN) and brain stem discharges to low-frequency tones (Rose et al. 1967 ) and complex harmonic sounds such as vowels (Palmer et al. 1986; Winter and Palmer 1990) and in responses to amplitude-modulated tones (for a review, see Joris et al. 2004 ). More recently, information theoretic studies have revealed how spike timing can be used to detect (Gai and Carney 2008) or distinguish categories of arbitrary spiking patterns to arbitrary stimuli (Huetz et al. 2006; Schnupp et al. 2006 ). However, this last approach does not consider the role of the dynamic properties of neurons in the encoding of stimulus information. Stellate cells in the VCN are well characterized with respect to both their biophysical and coding properties. These cells exhibit highly regular spiking (chopping response) in response to constant stimulation (for both current steps and pure tones) (Manis and Marx 1991; Rhode et al. 1983) . They also encode the frequency of AM using the temporal pattern of firing: they display a band-pass vector strength (VS) (Rhode and Greenberg 1994) and their interspike interval (ISI) statistics are related to the temporal periodicity of the stimuli presented (Wiegrebe and Winter 2001). These response properties are thought to result from summation of the inputs from auditory nerve fibers, temporal integration, and a simple spiking mechanism. Simulations of Hodgkin-Huxley (HH) type (Banks and Sachs 1991; Wang and Sachs 1995) or integrate-and-fire models (Hewitt et al. 1992) , reproducing the linear subthreshold current-voltage (I-V) curve of stellate cells, have successfully replicated their responses to pure tone at characteristic frequency (CF), the VS in response to AM tones and the responses to other periodic stimuli. In this article, we complement previous simulation studies using a mathematical theory explaining how nonlinear dynamical systems synchronize to time varying input. We observe higher-order temporal patterns, called "mode-locked" in response to several different classes of periodic stimuli: AM tones, steady-state vowels, and cosine-phase harmonic complexes. Mode-locking, of which phase-locking is a subset, results from the interaction between the dynamics of a nonlinear oscillator and a periodic stimulus. Such spiking patterns have been previously described in generic neuron models similar to models of stellate cells [for instance HH (Aihara et al. 1984; Lee and Kim 2006) or leaky integrate-and-fire (LIF) (Brette 2004; Coombes and Bressloff 1999; Keener et al. 1981) ] and have been observed in vitro under DC injection (Aihara et al. 1984; Brumberg and Gutkin 2007; Guttman et al. 1980; Shreiber et al. 2004). Mode-locked responses are often stable across regions of parameter space called Arnold tongues (for a review, see Pikovsky et al. 2001 ). Our report is the first description of mode-locking in the auditory system and under sensory stimulation in vivo. M E T H O D S Experimental data collection The data were collected from 54 healthy adult pigmented guinea pigs (Cavia porcellus), weighing in the range of 300 -400 g, which also provided extensive data for other studies. We analyzed the responses of 11 cells (not previously published) to SAM tones of 3-s duration presented 10 times with a range of modulation frequencies. Seven of these cells were classified as chopper units, two as onset choppers, and two as unusual. We also analyzed the responses of 24
doi:10.1152/jn.00070.2009 pmid:20042702 pmcid:PMC2887620 fatcat:cwsi5tzex5hqjlzx3gkff6v45i