Representation of high bandwidth sensory information by small circuits in the whisker system Rasmus Petersen Workshop on Computational Neuroscience, Warwick Dec 2008 Two views of neural coding • Low bandwidth e.g., visual cortex • High bandwidth e.g., fly H1 de Ruyter et al (1997) A1 α A2 A3 B1 β A4 B2 B3 C1 γ B4 C2 C3 D1 δ C4 C6 C5 C7 D8 D7 D2 D3 D6 D5 D4 E9 E8 E7 E1 E6 E2 E3 E4 E5 SI barrels barreloids Thalamus Brainstem barrelettes Brecht (2007) COIN Helmstaedter et al. (2007) Br Res Rev Tansu Celikel 30 micron grooves smooth 1 2 3 4 5 A Single whisker discrimination B C D E Carvell & Simons (1990) 10000 neurons per barrel SI 250 neurons per barreloid Thalamus Brainstem 250 neurons per barrelette 150 receptors per whisker micromotions free whisking Whisker position Whisker velocity Whisker acceleration object contact • Experimentally measured micromotions • Importance of temporal domain Arabzadeh et al. (2005) Coding temporal signals SI Thalamus Brainstem 1. Response question: What is the ‘information-bearing element’ of the neuronal response? 2. Stimulus question: What stimulus features do the information-bearing elements signify? The information-bearing element of a spike train Hypothesis 1. Firing rate Hypothesis 2. Correlations between spikes Firing rate vs temporal correlations • Effect of correlations on encoded information (Icorr) How much does the presence of noise correlations change the information compared to a hypothetical neural system where the neuron has identical mean firing rate but zero noise correlations? (eg Schneidman et al., 2003) • Effect of correlations on decodable information (∆I) If a hypothetical downstream decoding circuit attempts to decode using a model that includes mean firing rates but ignores noise correlations, how much information will be lost? (Nirenberg et al., 2001) Montemurro et al (2007) J Neurophysiol Summary • For VPM neurons stimulated by white noise, key “information-bearing element” is firing rate • For most VPM neurons, higher order temporal correlations have minor impact What stimulus features does the firing rate signify? Approaches: •Pseudolinear model: •Spike-triggered averaging •Non-linear models: •Spike feedback (Paninski) model •Spike-triggered covariance analysis Linear Nonlinear Poisson (LNP) Model A C E Position sensor Velocity sensor Acceleration sensor 0.8 0.3 0.5 k (t ) = i=T / δt ‡” i = 0 s (t - i δ t ) f (i δ t ) r ( t ) = g [k ( t ) ] Stim amplitude (SD) 0.7 0.6 0.5 0.4 0.2 0.3 0.1 0.2 0 0.1 -0.1 0.4 0 -0.2 -0.1 0.3 -0.3 -0.2 0.2 -0.3 -0.4 0.1 -0.4 -0.5 -0.5 0 30 20 10 0 -10 B 30 -0.6 20 10 0 -10 D 30 20 10 0 -10 F 0.4 0.45 Position Velocity Acceler. r (t ) = g[ s (t )] r (t ) = g[ s(t ) - s (t - δt )] r (t ) = g[12 s (t ) - s (t - δt ) + 12 s (t - 2δt )] Stim amplitude (SD) 0.4 0.2 0.3 0.1 0.35 0.2 0.3 0.1 0 0.25 -0.1 0 -0.2 0.2 -0.1 0.15 0.1 0.05 0 30 20 10 0 -10 Pre-spike tim e (m s) -0.3 -0.2 -0.4 -0.3 -0.5 30 20 10 0 -10 Pre-spike tim e (m s) 30 20 10 0 -10 Pre-spike tim e (m s) 0.5 B Firing rate (spikes/s) Stim amp (SD) A 0.4 0.3 0.2 0.1 0 40 20 0 Pre-spike tim e (m s) C 20 15 10 5 -2 0 2 Feature coefficient (SD) D 0.2 0 -0.2 -0.4 40 20 0 Pre-spike tim e (m s) Firing rate (spikes/s) 0.4 Stim amp (SD) 25 60 50 40 30 20 10 0 -2 0 2 Feature coefficient (SD) Petersen et al (in press) Neuron How accurate is the LNP model? • Non-linear approaches: – Maximum likelihood fitting of spike feedback (Paninski) model – Spike-triggered covariance analysis Petersen et al (in press) Neuron B 0.8 Information (bits/spike) Information (bits/spike) A 0.6 0.4 0.2 0 0 0.8 0.6 0.4 0.2 0 10 20 Feature C 0 10 20 Feature D 12 1.2 10 1 Number units STA information (bits/spike) 1.4 0.8 0.6 0.4 0.2 8 6 4 2 0 0 0.5 1 STC inform ation (bits/spike) 0 1 2 3 4 Inform ation ratio (STC/STA) Petersen et al (in press) Neuron LNP model k (t ) = ‡” r (t) = g i= T / δ t i= 0 [k (t) s (t - i δ t ) f (i δ t ) ] Petersen et al (in press) Neuron Petersen et al (in press) Neuron Petersen et al (in press) Neuron Conclusions • VPM neurons reliably encode complex whisker motion • Key information-bearing element of response is firing rate on millisecond time-scale • High reliability permits small subcortical circuits to support demanding sensory processing • Most VPM neurons can be described by LNP models • VPM exhibits a distributed code for whisker motion Acknowledgements Michael Bale Marco Brambilla Andrea Alenda Marcelo Montemurro Liam Paninski Stefano Panzeri Miguel Maravall EXTRA