The Volley Theory and the Spherical Cell Puzzle
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Neuroscience 154 (2008) 65–76 THE VOLLEY THEORY AND THE SPHERICAL CELL PUZZLE P. X. JORISa* AND P. H. bSMITH proved to dovetail very well with the physiological parcel- aLaboratory of Auditory Neurophysiology, K.U.Leuven, Campus GHBlation of response categories based on responses to short O&N2, Herestraat 49 bus 1021, B-3000 Leuven, Belgium tone bursts Kiang( et al., 1965a; Pfeiffer,). 1966Other bDepartment of Anatomy, University of Wisconsin–Madison, 1300 Uni-studies lent further credence to Osen’s scheme in terms of versity Avenue, Madison, WI, USA projections patterns Warr,( 1982) and intrinsic electrical properties Oertel,( 1999). Osen’s insightful observations have thus served as an organizational principle which Abstract—Temporal coding in the auditory nerve is strikingly transformed in the cochlear nucleus. In contrast to fibersenabled in the remarkable progress in the understanding of the auditory nerve, some neurons in the cochlear nucleusthis nucleus in the 1970s and 1980s. can show “picket fence” phase-locking to low-frequency The study of the CN highlights one of the most inter- pure tones: they fire a precisely timed action potentialesting at features of the auditory system: its morphological every cycle of the stimulus. Such synchronization enhance-and physiological specializations to process temporal in- ment and entrainment is particularly prominent in neuronsformation in the acoustic waveform. We focus here on with the spherical and globular morphology, described temporalby processing and two neuron types, called the Osen [Osen KK (1969) Cytoarchitecture of the cochlear nuclei spherical and globular cells by Osen, and point out an in the cat. J Comp Neurol 136:453– 483]. These neurons re- ceive large axosomatic terminals from the auditory nerve—unsolved puzzle. the end bulbs and modified end bulbs of Held—and project to binaural comparator nuclei in the superior olivary complex. THE VOLLEY THEORY The most popular model to account for picket fence phase- locking is monaural coincidence detection. This mechanismOne hundred years ago, Lord RayleighStrutt, 1907( ) is plausible for globular neurons, which receive a large showednum- a relationship between the perceptual localization ber of inputs. We draw attention to the existence of enhancedof sound and the interaural phase of tones at the two ears. phase-locking and entrainment in spherical neurons, whichEven earlier,Thompson (1877) had described the sensi- receive too few end-bulb inputs from the auditory nerve to tivity of humans to ongoing interaural phase differences for make a coincidence detection of end-bulb firings a plausible mechanism of synchronization enhancement. © 2008 IBRO.low-frequency tones. These observations established un- Published by Elsevier Ltd. All rights reserved. equivocally that temporal information at the two ears is accessed by the CNS and that it is used in spatial percep- Key words: temporal coding, binaural, synchronization, am-tion. These early pioneers thereby provided strong support plitude modulation, cochlear nucleus, jitter. for the “telephone” theory, as opposed to the “resonance” theory: theories which can be traced back to Helmholtz Contents and Rutherford and which today are referred to as tempo- The volley theory 65 ral and place coding. Single unit phase-locking and Besides the binaural psychophysical observations, its enhancement 66 Relationship to morphological cell types in CN there68 was also physiological evidence for the telephone Mechanisms of synchronization enhancement 7 0theory (seeDavis, 1984for an interesting personal histor- The puzzle of enhanced synchronization in SBCs ical72 account). Early recordings of gross evoked potentials Acknowledgments 73 showed responses that phase-locked to the stimulus References 73 waveform up to several WeverkHz ( and Bray, 1930a). Investigators puzzled over this for two reasons. First, it was Biological taxonomy is always fraught with splitting knownvs. from single cell recording in other systems that lumping difficulties. Kirsten Osen’s morphological parcel-neurons display refractory behavior and are limited in their firing rates to a few hundred spikes per second (microelec- lation of the cochlear nucleus Osen,(CN) 1969( ) was a trode recordings from single auditory neurons only became landmark achievement because it hit exactly the right level available much later: Galambos and Davis, 1943; Tasaki, along the splitter-lumper dimension. Her parcellation 1954). How could auditory neurons have temporal infor- *Corresponding author. Tel: ϩ32-16-34-57-41; fax: ϩ32-16-34-59-93. mation above frequencies corresponding to “normal” firing E-mail address: [email protected] (P. X. Joris). Abbreviations: AN, auditory nerve; AVCN, anteroventral cochlear nu- rates? Second, how could neurons be phase-locked and at cleus; CF, characteristic frequency; CN, cochlear nucleus; GBC, glob- the same time carry intensity information in their discharge ular bushy cell; ITD, interaural time difference; LSO, lateral superior rate? The latter was seen as a requirement based on olive; MNTB, medial nucleus of the trapezoid body; MSO, medial observations in other sensory systems (Adrian, 1928). The superior olive; SBC, spherical bushy cell; SOC, superior olivary com- plex; TB, trapezoid body; VCN, ventral cochlear nucleus; VNLL, ven- volley theory (Wever and Bray, 1930b) solved these diffi- tral nucleus of the lateral lemniscus; VS, vector strength. culties and argued that the resonance and telephone the- 0306-4522/08$32.00ϩ0.00 © 2008 IBRO. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.neuroscience.2008.03.002 65 66 P. X. Joris and P. H. Smith / Neuroscience 154 (2008) 65–76 ories were not mutually exclusive. Wever and Bray rea- 1975; Rhode and Smith, 1986; Rhode and Kettner, 1987; soned that single fibers can be synchronized to the stim- Joris et al., 1994a). Both components, high VS and en- ulus waveform even if they do not fire at every stimulus trainment, likely contribute to the strongly phase-locked cycle, and that the combined output of a group of fibers can gross potentials measured in the CNS (Boudreau, 1965). carry the temporal waveform in a volley of spikes. In their The combination of enhanced phase-locking and entrain- words, “The situation is something like beating a tattoo with ment means that these neurons can be described as “vol- the two hands working alternately, and establishing a total ley-detectors”: they seem to collect phase-locked spikes frequency double that of either hand” (Wever and Bray, from a group of AN inputs to produce a precise pulse train 1930b). Here we illustrate that the temporal code which is at the stimulus frequency (Fig. 2D). distributed over different fibers at the level of the auditory Fig. 1 illustrates phase-locking for an AN fiber and a nerve (AN) is transformed at successive synaptic levels to VCN neuron, tuned to the same frequency of 670 Hz (A). a more robust code at the single cell level. Fig. 1B and C shows dot rasters in response to 50 short tones at this frequency. There is a vertical alignment of SINGLE UNIT PHASE-LOCKING AND dots in both cases, but clearly this alignment is better in C. The red dots indicate spike times which are identical, ITS ENHANCEMENT within a 50 s window, across responses to at least two Computer-aided AN recordings (Kiang et al., 1965b; Rose stimulus presentations (of the 50 shown): for the black dots et al., 1967; Johnson, 1980) systematically demonstrated there is no matching spike time in any of the other spike phase-locking at frequencies far higher than maximal firing trains. The VCN neuron (C) tends to fire a spike on every rates sustained by AN fibers, which are ϳ300 Hz. As cycle over a narrow phase-range of the sinusoidal stimulus hypothesized by Wever and Bray (1930b), AN fibers skip waveform, resulting in a preponderance of spike times that cycles, even at very low frequencies, and the upper limit of are coincident across stimulus repetitions. The AN neuron phase-locking is thus not imposed by refractoriness (even is more stochastic in its firing, often skipping one, two, or though this statement is still encountered, e.g. Shepherd, more cycles, and the spikes are less well aligned across 1994). The most popular metric used to quantify phase- repetitions. The cycle histograms (Fig. 1D, E) show the locking is the vector strength (VS, Goldberg and Brown, instantaneous discharge rate directly as a function of stim- 1969). Spikes randomly distributed with respect to phase ulus phase. A flat distribution would indicate an absence of result in a VS near 0, while spikes occurring at a fixed phase-locking at the frequency of the histogram. There is phase yield values near 1 (Fig. 1). With this measure, phase-locking in both fibers, but there is more dispersion in phase-locking in the AN shows a low-pass characteristic the AN response. The same distributions are also shown in with an upper limit of ϳ4–5 kHz in the cat (Johnson, 1980; polar format, from which an averaged vector can be cal- Joris et al., 1994a) and somewhat lower in rodents (Palmer culated. The magnitude of this vector, normalized for the and Russell, 1986; Paolini et al., 2001; Taberner and Liber- overall discharge rate, is the VS and is much higher for the man, 2005). The exact limiting step(s) at the level of the VCN fiber (0.93) than for the AN fiber (0.64). Despite a cochlea are not known, but a number of candidate pro- stimulus frequency that is high relative to “routine” neuro- cesses such as hair cell membrane capacitance have nal firing rates, this VCN neuron also showed entrainment. been proposed (Palmer and Russell, 1986; Weiss and This is illustrated by the dominance of inter-spike intervals Rose, 1988). equal to the stimulus period (Fig. 1G), while the AN fiber Phase-locking changes in quality in the ascending au- shows a multimodal distribution (Fig. 1F) indicating fre- ditory system. Generally, there is a decrease in the upper quent skipping of stimulus cycles.