How is the stimulus represented in the nervous system?
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1 How is the stimulus represented in the nervous system? Eric Young F Rieke et al Spikes MIT Press (1997) Especially chapter 2 I Nelken et al Encoding stimulus information by spike numbers and mean response time in primary auditory cortex J Comput Neurosci 19: (2005) The fundamental assumption is that the representation is in terms of spike times (as opposed to subthreshold potentials for example) For the analysis, the spike train is reduced to a series of time points, the times at which action potentials occur A basic analysis: how did the neuron respond to the stimulus? DK Ryugo
2 But there are two different problems: (1) characterizing the response to a given stimulus (2) inferring the stimulus given a particular response Note they are different! Characterizing the stimulus given the response Characterizing the response, given the stimulus The stimulus (optical flow velocity) The response (number of spikes in 02 s) Rieke et al 1997 In principal, the two kinds of descriptions are interconvertible using Baye s theorem: measure in an experiment P(v n) = P(n,v) P(n) and so P(n v)p(v) P(v n) = P(n) The problem comes in estimating P(v) and P(n) which may be difficult to do meaningfully, especially for natural stimuli Thus we often work on the forward problem, estimating the response given an arbitrary stimulus, and postpone the reverse problem There is another problem: what is the appropriate variable to use for n, the response? Number of spikes is easy, but other measures which include spike times may be more appropriate
3 The stimulus is represented by the strength of firing (ie the discharge rate) or by some aspect of spike timing Usually there is more information in the latter stimulus spike train time rate code: different number of spikes, depending on the stimulus stimulus (expanded time scale) spike train (note phase locking of the spikes to the stimulus waveform) Any representation is based on population responses, ie on the distribution of activity in the array of neurons In hearing that means a tonotopic representation, by frequency The idea of a tonotopic representation is illustrated by the rate representation of sound spectrum in the auditory nerve, in this case for the vowel /eh/, as in met The plots show discharge rate in a large population of auditory nerve fibers, plotted versus best frequency The lines are smoothed versions of the data points individual fibers' rates Sachs and Young, 1979
4 Spike timing in the stimulus response can contribute to the representation in the brain (1) Note the periodic responses at the frequencies of components of the stimulus (eg F1, F2, and F3 for the /da/ below) Using this information requires a central processor sensitive to temporal patterns (2) The transitions along the frequency axis from one component of the stimulus to the next could serve as cues readable by central coincidence detectors (3) Similarly relative latency across BF could be used, discussed later Shamma 1985 from Miller and Sachs 1983 A temporal representation need not reflect the actual waveform of the stimulus, as in the previous example Neurons also code aspects of the stimulus by changing the overall temporal patterns of response Neurons in auditory cortex show different patterns of response depending on sound source direction A neural network model was trained to compute source azimuth from PSTs of neurons responses This worked pretty well Middlebrooks et al 1998
5 The analyses described above require assumptions about the nature of the representation To minimize the effects of assumptions, search for the optimal stimulus for a neuron, ie the stimulus to which the neuron responds most strongly One approach to finding the optimal stimulus is to use reverse correlation, in which the neuron is presented with rich ensemble of stimuli (noise) and signals its optimum by where it spikes C In auditory nerve fibers, averaging the stimulus preceding spikes finds short tone bursts at the BF of the neuron, with Fourier transforms that look like tuning curves, a comforting result Young et al 2005, Carney and Yin 1988 In the CNS, reverse correlation is applied by averaging the power spectrum of the stimulus preceding spikes (called the spectro-temporal receptive field, STRF) The results are more complex with excitatory and inhibitory areas This neuron did give strong responses to downsweeping tones decharms et al 1998
6 Although it is a seductive idea, the optimal stimulus may not be so useful First, it may not produce a predictive model Second, neurons may not have a true optimum For example, if rate depends on both linear and 2nd order weighting of the stimulus spectrum: r = R 0 +! w j S( f j ) +!! m jk S( f j )S( f k ) j j Then the rate response can have a maximum, a saddle, or a ridge In these cases, the optimization method may fail in confusing ways k DiMattina and Zhang, 2009 The saddle behavior occurs in neurons in the dorsal cochlear nucleus DiMattina, Anderson, Young, Zhang, 2010
7 Moreover, the optimal stimulus derived in this way may be different depending on the stimulus ensemble used to derive it In these cases, the STRF is not a unique characterization of the neuron, probably because of the nonlinearity of the neuron s responses Theunissen et al 2000 Everything up to now has been aimed at estimating P(n v), the response given the stimulus To approach the estimation of P(v n), one approach is to use the neuron s responses to show how it maps the stimulus space The stimulus dimensions that the neuron represents are those that induce a change in its responses The stimuli the spike trains P 1 P 2 similar spike trains P 3 P 4 not This neuron considers stimuli P1 and P3 to be similar, but stimuli P3 and P4 to be different P n
8 A simple example: which auditory nerve fibers signal the difference between two vowel spectra, based just on discharge rate? The answer is the fibers with BFs near the formants, where the vowels differ Miller et al 1999 It is useful to be able to measure the information that neurons responses provide about the stimulus Define information as the reduction in uncertainty about an event, where uncertainty is measured by entropy? Which stimulus was presented? The possibilities and their probabilities P 1 P 2 The uncertainty about the stimulus or entropy H is H =! n " i=1 P i log 2 P i P 3 P 4 Then the information provided by the spike trains about the stimulus is the reduction in entropy: MI = H (S)! H (S R) P n called the mutual information or MI
9 An example, trying to discover what aspects of a stimulus neurons are responding to, when the responses are very poorly time-locked Responses in insula versus A1 to a variety of natural stimuli The insula responses bear only a general relationship to the stimuli A monkey call modified in three ways Insula neurons provide more information about the calls than the modified ones Remedios et al 2009 Neurons can represent multiple cues in their discharge rates This raises the question of how different sources of information can be simultaneously represented by a neuron For example, in the inferior colliculus: ILD and SN sensitive SN, ILD and ITD sensitive May, Davis, Ramachandran
10 Of course, neurons are encoding many features of the stimulus simultaneously (frequency content, loudness, temporal parameters, modulation, But rate can only code one thing at a time! confounded information Type I and O neurons vary from SNdominated to ILDdominated Type V neurons devote little MI to SN All types can encode ITD and vary in the relative encoding of ITD and ILD (BFs<4 khz only) Type V neurons encode mainly ABI, whereas type O and type I units encode ILD Which aspect of a neuron s response provides the most information about the stimulus? 1 discharge rate (previous slides) 2 latency of the first spike 3 temporal spiking patterns Note that these are quite different Chase and Young 2006
11 The information contained in spike timing patterns can be analyzed using a method due to Victor and Purpura, Distances between spike trains are computed 2 From the distances a cluster analysis can be done 3 The result is a confusion matrix from which the MI can be calculated Chase and Young 2006 Considering spike timing patterns increases the information in spike trains over that due to rate The extra information encoded in spike timing Chase and Young 2008
12 Population responses to two tones Note 1 Wide distribution of responses along the BM 2 Two tone suppression of responses to one tone by the other (*) 3 Generation of combination tones at frequencies f 2 -f 1 and 2f 1 -f 2 Even though there is no energy in the stimulus at these frequencies, they distribute along the BM like real tones Presumably energy at these frequencies is generated by BM nonlinearity * 217 and 279 khz at 65 db SPL Kim et al 1975
13 A better representation is provided by looking at the strength of phase locking at various BFs With this measure, it is possible to tell which of the many frequency components of the vowel produces the response of a particular fiber Stimulus frequency to which the fiber responds Strength of the response Where on the basilar membrane? Miller et al 1997
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