Temporal population code of concurrent vocal signals in the auditory midbrain

Unique patterns of spike activity across neuron populations have been implicated in the coding of complex sensory stimuli. Delineating the patterns of neural activity in response to varying stimulus parameters and their relationships to the tuning characteristics of individual neurons is essential to ascertaining the nature of population coding within the brain. Here, we address these points in the midbrain coding of concurrent vocal signals of a sound-producing fish, the plainfin midshipman. Midshipman produce multiharmonic vocalizations which frequently overlap to produce beats. We used multivariate statistical analysis from single-unit recordings across multiple animals to assess the presence of a temporal population code. Our results show that distinct patterns of temporal activity emerge among midbrain neurons in response to concurrent signals that vary in their difference frequency. These patterns can serve to code beat difference frequencies. The patterns directly result from the differential temporal coding of difference frequency by individual neurons. Difference frequency encoding, based on temporal patterns of activity, could permit the segregation of concurrent vocal signals on time scales shorter than codes requiring averaging. Given the ubiquity across vertebrates of auditory midbrain tuning to the temporal structure of acoustic signals, a similar temporal population code is likely present in other species.     

Peripheral encoding of behaviorally relevant acoustic signals in a vocal fish: harmonic and beat stimuli

Nesting male midshipman fish, Porichthys notatus, emit simple, long-duration sounds known as hums, which are attractive to gravid females. While hums share the multi-harmonic structure typical of many vertebrate communication sounds, their lack of amplitude modulation gives individual hums unusually simple temporal envelopes. However, hums often overlap, producing beats in the summed acoustic waveform. This study presents responses of individual saccular afferent fibers to two-tone harmonic and beat stimuli presented via an underwater loudspeaker. Spike activity was quantified as vector strength of synchronization and average spike rate. Responses to harmonic stimuli depended on harmonic phase; these effects apparently resulted primarily from variation in waveform fine temporal structure rather than auditory non-linearities. At most phases, addition of the harmonic enhanced afferent synchronization compared to the fundamental alone. Two-tone beat stimuli evoked stronger synchronization to the component frequencies than to the beat modulation rate. Vector strength tended to be higher to the lower frequency component, and this pattern appeared to derive from afferent tuning. Midshipman saccular afferents encoded both the temporal envelope and waveform fine structure of these naturalistic signals, information that may be important in conspecific communication.     

Peripheral encoding of behaviorally relevant acoustic signals in a vocal fish: single tones

The midshipman fish, Porichthys notatus, generates acoustic signals for intraspecific communication. Nesting males produce long-duration “hums” which attract gravid females and can be effectively mimicked by pure tones. In this study we examine the encoding of tonal signals by the midshipman peripheral auditory system. Single-unit recordings were made from afferents innervating the sacculus while presenting sounds via an underwater loudspeaker. Units were characterized by iso-intensity spike rate and vector strength of synchronization curves, as well as by peri-stimulus time histograms. Additionally, response-intensity curves and responses to long-duration (up to 10 s) stimuli were obtained. As has been seen in other teleosts, afferents had highly variable activity profiles. Excitatory frequencies ranged from 60 to over 300 Hz with most units responding best around 70 or 140 Hz. Thresholds at 90 Hz ranged from 95 to 145 dB re 1 μPa. Strong synchronization provided a robust temporal code of frequency, comparable to that described for goldfish. Spike rate showed varying degrees of adaptation but high rates were generally maintained even for 10-s stimuli. The midshipman peripheral auditory system is well suited to encoding conspecific communication signals, but nonetheless shares many response patterns with the auditory system of other teleosts. Accepted: 10 February 1999     

Processing of Auditory Midbrain Interspike Intervals by Model Neurons

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.     

Neurons with different temporal firing patterns in the inferior colliculus of the little brown bat differentially process sinusoidal amplitude-modulated signals

We examined how well single neurons in the inferior colliculus (IC) of an FM bat (Myotis lucifugus) processed simple tone bursts of different duration and sinusoidal amplitude-modulated (SAM) signals that approximated passively heard natural sounds. Units' responses to SAM tones, measured in terms of average spike count and firing synchrony to the modulation envelope, were plotted as a function of the modulation frequency to construct their modulation transfer functions. These functions were classified according to their shape (e.g., band-, low-, high-, and all-pass). IC neurons having different temporal firing patterns to simple tone bursts (tonic, chopper, onset-late, and onset-immediate) exhibited different selectivities for SAM signals. All tonic and 83% of chopper neurons responded robustly to SAM signals and displayed a variety of spike count-based response functions. These neurons showed a decreased level of time-locking as the modulation frequency was increased, and thereby gave low-pass synchronization-based response functions. In contrast, 64% of onset-immediate, 37% of onset-late and 17% of chopper units failed to respond to SAM signals at any modulation frequency tested (5–800 Hz). Those onset neurons that did respond to SAM showed poor time-locking (i.e., non-significant levels of synchronization). We obtained evidence that the poor SAM response of some onset and chopper neurons was due to a preference for short-duration signals. These data suggest that tonic and most chopper neurons are better-suited for the processing of long-duration SAM signals related to passive hearing, whereas onset neurons are better-suited for the processing of short, pulsatile signals such as those used in echolocation.Abbreviations C chopper - FM frequency-modulated - IC inferior colliculus - MTF modulation transfer function - O₁ onset-immediate - O_L onset-late - PAM pulsatile amplitude-modulation - PSTH peri-stimulus time histogram - SAM sinusoidal amplitude-modulation - SC synchronization coefficient - T tonic     

Changes in response latencies of the mouse inferior colliculus neurons depending on the position and movement direction of the spectral contrast

Variability of response latency of neurons in the mouse inferior colliculus of (Mus musculus) to signals of notch noise and of noise band with regular varying of the notch/band center frequencies, have been studied. Plots of latency and spike count versus notch/band center frequency were constructed (latency functions and spike count functions). Spectral notch/noise band motion crossing boundaries of excitatory areas in the neurons frequency receptive field could produce latency function shifts (and appropriate to this spike count function shifts). Direction-dependent latency function and spike count function shifts were mostly seen for primary-like and V-shape neurons. The most interesting feature of directional sensitivity of inhibitory-dominated neurons was the selective shortening of latency and selective synchronization of the initial spikes (with appropriate to this spike count rise). The dynamic properties of inhibitory-dominated neurons can be explained on the basis of their selective sensitivity to position of spectral contrast in frequency receptive field, connected with disinhibition, and of the character of distribution of excitatory and inhibitory inputs. Manifestation of motion effects was influenced by spectral shape of noise signal and notch width.     

Temporal processing of vibratory communication signals at the level of ascending interneurons in Nezara viridula (Hemiptera: Pentatomidae)

During mating, males and females of N. viridula (Heteroptera: Pentatomidae) produce sex- and species-specific calling and courtship substrate-borne vibratory signals, grouped into songs. Recognition and localization of these signals are fundamental for successful mating. The recognition is mainly based on the temporal pattern, i.e. the amplitude modulation, while the frequency spectrum of the signals usually only plays a minor role. We examined the temporal selectivity for vibratory signals in four types of ascending vibratory interneurons in N. viridula. Using intracellular recording and labelling technique, we analyzed the neurons' responses to 30 pulse duration/interval duration (PD/ID) combinations. Two response arrays were created for each neuron type, showing the intensity of the responses either as time-averaged spike counts or as peak instantaneous spike rates. The mean spike rate response arrays showed preference of the neurons for short PDs (below 600 ms) and no selectivity towards interval duration; while the peak spike rate response arrays exhibited either short PD/long ID selectivity or no selectivity at all. The long PD/short ID combinations elicited the weakest responses in all neurons tested. No response arrays showed the receiver preference for either constant period or duty cycle. The vibratory song pattern selectivity matched the PD of N. viridula male vibratory signals, thus pointing to temporal filtering for the conspecific vibratory signals already at level of the ascending interneurons. In some neurons the responses elicited by the vibratory stimuli were followed by distinct, regular oscillations of the membrane potential. The distance between the oscillation peaks matched the temporal structure of the male calling song, indicating a possible resonance based mechanism for signal recognition.     

Adaptation of differential sensitivity of auditory system neurons to amplitude modulation after abrupt change of signal level

Impulse activity of neurons of brainstem auditory nuclei (medulla dorsal nucleus and midbrain torus semicircularis) of the grass frog (Rana temporaria) was recorded under action of long amplitude-modulated tonal signals. After adaptation of neuronal response to acting stimulus (30–60 s after its onset), we performed a sharp change (by 20–40 dB) of the mean signal level with preservation of unchanged frequency and depth of modulation. We also recorded a change of density impulsation and of degree of its synchronization with the modulation period as well as the phase of maximum reaction at the modulation period and phase of the response every 2 or 4 s. In the adapted state, the sharp change of the mean level had been provided, while maintaining frequency and depth unchanged. During the adaptation to long signals with small modulation indexes the firing rate continuously decreased, but synchronization with envelope usually increased considerably. A sharp rise in the mean level resulted in an increase of firing rate, which could be accompanied either by a continuation of synchronization growth (the effect is more typical of the dorsal nucleus) or by a sharp fall in synchrony with its subsequent slow recovery (the effect is more typical of the torus semicircularis). Nature of the changes following the change of the intensity of the reaction could depend on the signal parameters (initial level, magnitude of the jump, frequency and depth of modulation). The connection between the observed physiological data and the psychophysics of differential intensity coding is discussed.     

Developmental experience alters information coding in auditory midbrain and forebrain neurons

In songbirds, species identity and developmental experience shape vocal behavior and behavioral responses to vocalizations. The interaction of species identity and developmental experience may also shape the coding properties of sensory neurons. We tested whether responses of auditory midbrain and forebrain neurons to songs differed between species and between groups of conspecific birds with different developmental exposure to song. We also compared responses of individual neurons to conspecific and heterospecific songs. Zebra and Bengalese finches that were raised and tutored by conspecific birds, and zebra finches that were cross‐tutored by Bengalese finches were studied. Single‐unit responses to zebra and Bengalese finch songs were recorded and analyzed by calculating mutual information (MI), response reliability, mean spike rate, fluctuations in time‐varying spike rate, distributions of time‐varying spike rates, and neural discrimination of individual songs. MI quantifies a response's capacity to encode information about a stimulus. In midbrain and forebrain neurons, MI was significantly higher in normal zebra finch neurons than in Bengalese finch and cross‐tutored zebra finch neurons, but not between Bengalese finch and cross‐tutored zebra finch neurons. Information rate differences were largely due to spike rate differences. MI did not differ between responses to conspecific and heterospecific songs. Therefore, neurons from normal zebra finches encoded more information about songs than did neurons from other birds, but conspecific and heterospecific songs were encoded equally. Neural discrimination of songs and MI were highly correlated. Results demonstrate that developmental exposure to vocalizations shapes the information coding properties of songbird auditory neurons. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 70: 235–252, 2010.     

Auditory information coding by modeled cochlear nucleus neurons

In this paper we use information theory to quantify the information in the output spike trains of modeled cochlear nucleus globular bushy cells (GBCs). GBCs are part of the sound localization pathway. They are known for their precise temporal processing, and they code amplitude modulations with high fidelity. Here we investigated the information transmission for a natural sound, a recorded vowel. We conclude that the maximum information transmission rate for a single neuron was close to 1,050 bits/s, which corresponds to a value of approximately 5.8 bits per spike. For quasi-periodic signals like voiced speech, the transmitted information saturated as word duration increased. In general, approximately 80% of the available information from the spike trains was transmitted within about 20 ms. Transmitted information for speech signals concentrated around formant frequency regions. The efficiency of neural coding was above 60% up to the highest temporal resolution we investigated (20 μs). The increase in transmitted information to that precision indicates that these neurons are able to code information with extremely high fidelity, which is required for sound localization. On the other hand, only 20% of the information was captured when the temporal resolution was reduced to 4 ms. As the temporal resolution of most speech recognition systems is limited to less than 10 ms, this massive information loss might be one of the reasons which are responsible for the lack of noise robustness of these systems.     

Rates and rhythms: a synergistic view of frequency and temporal coding in neuronal networks

In the CNS, activity of individual neurons has a small but quantifiable relationship to sensory representations and motor outputs. Coactivation of a few 10s to 100s of neurons can code sensory inputs and behavioral task performance within psychophysical limits. However, in a sea of sensory inputs and demand for complex motor outputs how is the activity of such small subpopulations of neurons organized? Two theories dominate in this respect: increases in spike rate (rate coding) and sharpening of the coincidence of spiking in active neurons (temporal coding). Both have computational advantages and are far from mutually exclusive. Here, we review evidence for a bias in neuronal circuits toward temporal coding and the coexistence of rate and temporal coding during population rhythm generation. The coincident expression of multiple types of gamma rhythm in sensory cortex suggests a mechanistic substrate for combining rate and temporal codes?on the basis of stimulus strength.     

Sex recognition and neuronal coding of electric organ discharge waveform in the pulse-type weakly electric fish, Hypopomus occidentalis

1. Hypopomus occidentalis, a weakly electric gymnotiform fish with a pulse-type discharge, has a sexually dimorphic electric organ discharge (Hagedorn 1983). The electric organ discharges (EODs) of males in the breeding season are longer in duration and have a lower peak-power frequency than the EODs of females. We tested reproductively mature fish in the field by presenting electronically generated stimuli in which the only cue for sex recognition was the waveshape of individual EOD-like pulses in a train. We found that gravid females could readily discriminate male-like from female-like EOD waveshapes, and we conclude that this feature of the electric signal is sufficient for sex recognition. 2. To understand the possible neural bases for discrimination of male and female EODs by H . occidentalis, we conducted a neurophysiological examination of both peripheral and central neurons. Our studies show that there are sets of neurons in this species which can discriminate male or female EODs by coding either temporal or spectral features of the EOD. 3. Temporal encoding of stimulus duration was observed in evoked field potential recordings from the magnocellular nucleus of the midbrain torus semicircularis. This nucleus indirectly receives pulse marker electroreceptor information. The field potentials suggest that comparison is possible between pulse marker activity on opposite sides of the body. 4. From standard frequency-threshold curves, spectral encoding of stimulus peak-power frequency was measured in burst duration coder electroreceptor afferents. In both male and female fish, the best frequencies of the narrow-band population of electroreceptors were lower than the peak-power frequency of the EOD. Based on this observation, and the presence of a population of wide-band receptors which can serve as a frequency-independent amplitude reference, a slope-detection model of frequency discrimination is advanced. 5. Spectral discrimination of EOD peak-power frequency was also shown to be possible in a more natural situation similar to that present during behavioral discrimination. As the fish's EOD mimic slowly scanned through and temporally coincided with the neighbor's EOD mimic, peak spike rate in burst duration coder afferents was measured. Spike rate at the moment of coincidence changed predictably as a function of the neighbor's EOD peak-power frequency. 6. Single-unit threshold measurements were made on afferents from peripheral burst duration coder receptors in the amplitude-coding pathway, and midbrain giant cells in the time-coding pathway.(ABSTRACT TRUNCATED AT 400 WORDS)     

Temporal peculiarities of responses of auditory system neurons of the frog <Emphasis Type="Italic">Rana temporaria</Emphasis> to tone bursts with different modulation frequencies

Activity of medullar and midbrain auditory neurons at action of amplitude-modulated tone burst was recorded in immobilized common frogs Rana temporaria. Depth of modulation amounted to 10% or 80%, frequency of modulation varied from 5 to 150 Hz, and carrier intensity was in the range of 20–30 dB. Phasic neurons in medulla clearly reproduced the modulation frequency, but only at the 80% modulation depth. However, during presentation of signal with the 10% modulation depth, these neurons practically did not respond. Tonic neurons were able to reproduce the modulation frequency up to 10–150 Hz, but at the 10% modulation depth, the degree of reproduction of envelope was rather low, although for several first modulation periods it rose statistically significantly. In midbrain, the highest frequency of the reproduced modulation sharply fell. At greater modulation frequencies, the response of these neurons qualitatively reminds that of medullar neurons. At the low modulation frequencies, there is identified a group of midbrain neurons with a prominent increase of the signal modulation. This occurs in the frequency diapason up to 60 Hz; at an increase of the modulation frequency the time of achievement of maximal synchronization decreases. The optimal modulation frequency in many neurons of semicircular torus corresponds to parameters of the male nuptial call.     

Ion channel noise can explain firing correlation in auditory nerves

Sensory neurons code information about stimuli in their sequence of action potentials (spikes). Intuitively, the spikes should represent stimuli with high fidelity. However, generating and propagating spikes is a metabolically expensive process. It is therefore likely that neural codes have been selected to balance energy expenditure against encoding error. Our recently proposed optimal, energy-constrained neural coder (Jones et al. Frontiers in Computational Neuroscience, 9, 61 2015) postulates that neurons time spikes to minimize the trade-off between stimulus reconstruction error and expended energy by adjusting the spike threshold using a simple dynamic threshold. Here, we show that this proposed coding scheme is related to existing coding schemes, such as rate and temporal codes. We derive an instantaneous rate coder and show that the spike-rate depends on the signal and its derivative. In the limit of high spike rates the spike train maximizes fidelity given an energy constraint (average spike-rate), and the predicted interspike intervals are identical to those generated by our existing optimal coding neuron. The instantaneous rate coder is shown to closely match the spike-rates recorded from P-type primary afferents in weakly electric fish. In particular, the coder is a predictor of the peristimulus time histogram (PSTH). When tested against in vitro cortical pyramidal neuron recordings, the instantaneous spike-rate approximates DC step inputs, matching both the average spike-rate and the time-to-first-spike (a simple temporal code). Overall, the instantaneous rate coder relates optimal, energy-constrained encoding to the concepts of rate-coding and temporal-coding, suggesting a possible unifying principle of neural encoding of sensory signals.     

Cerebellar Nuclear Neurons Use Time and Rate Coding to Transmit Purkinje Neuron Pauses

Neurons of the cerebellar nuclei convey the final output of the cerebellum to their targets in various parts of the brain. Within the cerebellum their direct upstream connections originate from inhibitory Purkinje neurons. Purkinje neurons have a complex firing pattern of regular spikes interrupted by intermittent pauses of variable length. How can the cerebellar nucleus process this complex input pattern? In this modeling study, we investigate different forms of Purkinje neuron simple spike pause synchrony and its influence on candidate coding strategies in the cerebellar nuclei. That is, we investigate how different alignments of synchronous pauses in synthetic Purkinje neuron spike trains affect either time-locking or rate-changes in the downstream nuclei. We find that Purkinje neuron synchrony is mainly represented by changes in the firing rate of cerebellar nuclei neurons. Pause beginning synchronization produced a unique effect on nuclei neuron firing, while the effect of pause ending and pause overlapping synchronization could not be distinguished from each other. Pause beginning synchronization produced better time-locking of nuclear neurons for short length pauses. We also characterize the effect of pause length and spike jitter on the nuclear neuron firing. Additionally, we find that the rate of rebound responses in nuclear neurons after a synchronous pause is controlled by the firing rate of Purkinje neurons preceding it.     

Membrane Potential Fluctuations Determine the Precision of Spike Timing and Synchronous Activity: A Model Study

It is much debated on what time scale information is encoded by neuronal spike activity. With a phenomenological model that transforms time-dependent membrane potential fluctuations into spike trains, we investigate constraints for the timing of spikes and for synchronous activity of neurons with common input. The model of spike generation has a variable threshold that depends on the time elapsed since the previous action potential and on the preceding membrane potential changes. To ensure that the model operates in a biologically meaningful range, the model was adjusted to fit the responses of a fly visual interneuron to motion stimuli. The dependence of spike timing on the membrane potential dynamics was analyzed. Fast membrane potential fluctuations are needed to trigger spikes with a high temporal precision. Slow fluctuations lead to spike activity with a rate about proportional to the membrane potential. Thus, for a given level of stochastic input, the frequency range of membrane potential fluctuations induced by a stimulus determines whether a neuron can use a rate code or a temporal code. The relationship between the steepness of membrane potential fluctuations and the timing of spikes has also implications for synchronous activity in neurons with common input. Fast membrane potential changes must be shared by the neurons to produce synchronous activity.     

A model of the relation of tonotopy and synchronization in the auditory system

Tonotopy and synchronization of spike discharges with the stimulus frequency are two modes of coding which are probably not independent. After defining an appropriate process of coding and a measure of temporal correlations between two neighbouring channels, we show that it is possible to build with these two fundamental features of the auditory system, a neurophysiologically plausible neural network which has properties of noise resistance and signal segmentation.     

Warm body temperature facilitates energy efficient cortical action potentials

The energy efficiency of neural signal transmission is important not only as a limiting factor in brain architecture, but it also influences the interpretation of functional brain imaging signals. Action potential generation in mammalian, versus invertebrate, axons is remarkably energy efficient. Here we demonstrate that this increase in energy efficiency is due largely to a warmer body temperature. Increases in temperature result in an exponential increase in energy efficiency for single action potentials by increasing the rate of Na(+) channel inactivation, resulting in a marked reduction in overlap of the inward Na(+), and outward K(+), currents and a shortening of action potential duration. This increase in single spike efficiency is, however, counterbalanced by a temperature-dependent decrease in the amplitude and duration of the spike afterhyperpolarization, resulting in a nonlinear increase in the spike firing rate, particularly at temperatures above approximately 35°C. Interestingly, the total energy cost, as measured by the multiplication of total Na(+) entry per spike and average firing rate in response to a constant input, reaches a global minimum between 37-42°C. Our results indicate that increases in temperature result in an unexpected increase in energy efficiency, especially near normal body temperature, thus allowing the brain to utilize an energy efficient neural code.     

Processing of behaviorally relevant temporal parameters of acoustic stimuli by single neurons in the superior olivary nucleus of the leopard frog

Summary Response characteristics of 130 single neurons in the superior olivary nucleus of the northern leopard frog (Rana pipiens pipiens) were examined to determine their selectivity to various behaviorally relevant temporal parameters [rise-fall time, duration, and amplitude modulation (AM) rate of acoustic signals. Response functions were constructed with respect to each of these variables. Neurons with different temporal firing patterns such as tonic, phasic or phasic-burst firing patterns, participated in time domain analysis in specific manners. Phasic neurons manifested preferences for signals with short rise-fall times, thus possessing low-pass response functions with respect to this stimulus parameter; conversely, tonic and phasic-burst units were non-selective and possessed all-pass response functions. A distinction between temporal firing patterns was also observed for duration coding. Whereas phasic units showed no change in the mean spike count with a change in stimulus duration (i.e., all-pass duration response functions), tonic and phasic-burst units gave higher mean spike counts with an increase in stimulus duration (i.e., primary-like high-pass response functions). Phasic units manifested greater response selectivity for AM rate than did tonic or phasic-burst units, and many phasic units were tuned to a narrow range of modulation rates (i.e., band-pass). The results suggest that SON neurons play an important role in the processing of complex acoustic patterns; they perform extensive computations on AM rate as well as other temporal parameters of complex sounds. Moreover, the response selectivities for rise-fall time, duration, and AM rate could often be shown to contribute to the differential responses to complex synthetic and natural sounds.Abbreviations SON superior olivary nucleus - DMN dorsal medullary nucleus - TS torus semicircularis - FTC frequency threshold curve - BF best excitatory frequency - PAM pulsatile amplitude modulation - SAM sinusoidal amplitude modulation - SQAM square-wave amplitude modulation - MTF modulation transfer function - PSTH peri-stimulus time histogram     

The role of spike timing in the coding of stimulus location in rat somatosensory cortex

Although the timing of single spikes is known to code for time-varying features of a sensory stimulus, it remains unclear whether time is also exploited in the neuronal coding of the spatial structure of the environment, where nontemporal stimulus features are fundamental. This report demonstrates that, in the whisker representation of rat cortex, precise spike timing of single neurons increases the information transmitted about stimulus location by 44%, compared to that transmitted only by the total number of spikes. Crucial to this code is the timing of the first spike after whisker movement. Complex, single neuron spike patterns play a smaller, synergistic role. Timing permits very few spikes to transmit high quantities of information about a behaviorally significant, spatial stimulus.