DOCSLIB.ORG

Neural Coding of Pleasure: “Rose-Tinted Glasses” of the Ventral Pallidum

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Neural Coding of Pleasure: “Rose-Tinted Glasses” of the Ventral Pallidum Copying or circulation without permission are strictly prohibited. This chapter is included in Kringelbach ML and Berridge KC, "Pleasures of the Brain" (c) 2010. Oxford University Press: New York. 3 Neural Coding of Pleasure: “Rose-tinted Glasses” of the Ventral Pallidum J. WAYNE ALDRIDGE AND KENT C. BERRIDGE leasure is not a sensation. What is it then? Nico to be addressed. The “pleasure gloss” metaphor, PFrijda’s answer in the “pleasure questions” sec- applied to the transformation of neural signals for a tion of this book (which he suggested a number of stimulus, is like a varnish that is applied on top of a years ago) epitomizes an emerging consensus among dull object to transform it into a shiny one. Adding many psychologists and neuroscientists (Frijda, hedonic tone to the signal passed on to downstream Chapter 6, this book). He notes that pleasure “is a structures, the neural gloss eL ectively gives the entire ‘pleasantness gloss’ added to whatever is pleasant.” brain a “rose-tinted” hedonic perception of the stim- Other chapter authors in this book describe plea- ulus as pleasant. sure similarly in their answers to “pleasure questions” I n t he cont ex t of neu r a l G r i n g s i g n a l s , ou r ide a i s t h at as “the subsequent valuation of sensory stimuli” a particular pattern of neuronal spikes or action poten- (Kringelbach, Chapter 12, this book); “integrated with tials in crucial neurons may apply a glaze of pleasure sensation” (Dickinson and Balleine, Chapter 4, this on what might otherwise be an ordinary sensation or book); or “arises from a weighted combination of the action signal. At the moment of such a signal, neural sensory signals” (Kringelbach, Chapter 12, this book; activity related to a potentially hedonic sensation will Leknes and Tracey, Chapter 19 this book). Pleasure as be comingled with signals that speciG cally implement a hedonic “gloss” (Frijda, Chapter 6, this book; Smith the pleasure gloss. It is the pleasure- generating neural et al., Chapter 1, this book) on sensations is a succinct pattern we wish to identify. A pleasure transforma- way to describe how brain signals representing mere tion might excite, inhibit, or vary the pattern of G r- sensations (or applied to behavior-generating signals, ing activity within the target structure it modulates actions) become glazed by coincident hedonic neural and as a result dynamically recruits changes in activity activity that imbues them with pleasure, transforming proG les throughout an entire circuit. The particular the signals into hedonic stimuli (or hedonic actions). pattern we will describe is an excitation in a large Thus, viewed through the brain’s metaphoric “rose- population of neurons within a hedonic hotspot of the tinted glasses of pleasure,” ordinary sensations become ventral pallidum. pleasurable sensations. This chapter will focus on neural activity pro- Here we ask: how is a “pleasure gloss” encoded G les in the ventral pallidum because we believe this in brain activity? Where in the brain is this glossing brain structure is particularly important to applying operation performed and how does it work? Is it possi- a hedonic gloss (Figure 3.1). This structure in the ble for neuroscientists to recognize the signature pat- subcortical forebrain is a nexus of circuits that pro- terns of neural activity that represent a pleasure gloss? cess emotion information. We will describe reasons These are di0 cult questions that are only beginning as to why we think the ventral pallidum is especially 62 MlKringelbach_BookPS.indb 62 4/27/2009 6:15:36 PM Copying or circulation without permission are strictly prohibited. This chapter is included in Kringelbach ML and Berridge KC, "Pleasures of the Brain" (c) 2010. Oxford University Press: New York. 63 Aldridge and Berridge: Neural Coding of Pleasure Cortex Hippocampus Cd Thalamus Cd/Put Put Nucleus GP Accumbens GP Ventral Tegmental VP Area VP Ventral Pallidum to Brainstem Amygdala Figure 3.1 Ventral pallidum—sketches of rat and human coronal sections (left and middle panels). Schematic in right panel shows major input and output pathways of ventral pallidum. likely to perform a hedonic transformation. It is worth from tasty food, a humorous joke, or from listening to noting that the ventral pallidum has only recently music requires learning and complex cognitive repre- become appreciated as a distinct neuroanatomical sentations, such as in orbitofrontal cortex, insula cor- entity, let alone one with special hedonic functions. tex, and anterior cingulate cortex (Blood and Zatorre, Older literature did not usually discuss the ven- 2001; Kringelbach, 2005; Watson et al., 2007). Thus, tral pallidum because it used to be considered as just the particular pattern of coactivated cortical circuits the ventral part of the globus pallidus (a component would resolve the high level cognitive features of a of the basal ganglia, which are brain structures that pleasantness gloss on sensations or actions. include the neostriatum, globus pallidus, entopedun- cular nucleus, subthalamic nucleus, and the substantia nigra in the midbrain ventral tegmentum). The basal Ventral Pallidum: Applying a ganglia were traditionally viewed as important to Pleasure Gloss to Sweetness? controlling movements, but now are also recognized as crucial for neural processing related to emotion, Still, for seeing the basic glazing operation by which motivation, and reward too. Especially important to the pleasure gloss is actually generated and applied to aL ective- motivational functions are particular com- sensations, the ventral pallidum has particular advan- ponents of basal ganglia such as ventral tegmentum tages. Here a special insight may be gained into why and its mesolimbic dopamine projections, the nucleus sugar tastes nice and how some other sensations can accumbens (formerly known as the ventral portion of become as nice as sugar, at least when they get the neostriatum), and the ventral pallidum. same neuronal hedonic gloss. We do not mean to exclude the importance of other Several reasons have led us to focus on the ven- brain structures. We focus on the ventral pallidum tral pallidum, in particular, for adding a pleasure gloss simply because it is a good place to start to understand to ongoing sensations via its neuronal G ring patterns. pleasure. Besides the basal ganglia, of course, many F i r s t , t he ve n t r a l p a l l i d u m c o n t a i n s a “ he d o n ic h o t s p o t ” other brain structures are also involved in assigning in its posterior half, a roughly cubic-millimeter brain pleasure (Kringelbach, 2005) (many of the chapters, site in which neuronal events can lead to ampliG ca- this book). Many of them might do so in cognitive and tions of a sensory pleasure (Peciña and Berridge, predictive ways that go beyond painting the basic plea- 2005; Peciña et al., 2006; Smith and Berridge, 2005, sure gloss onto a sensation. Much of human pleasure 2007; Smith et al., Chapter 1, this book). In hedonic has cognitive qualities that infuse uniquely human hotspots, microinjections of opioids and other neuro- properties, and it is likely that abstract or higher plea- chemicals are able to glaze an extra gloss of pleasure sures depend on cortical brain areas for those qual- onto sweet sensations, enhancing ‘liking’ responses. ities. For example, full pleasure derived by humans Several hotspots have recently been mapped in the MlKringelbach_BookPS.indb 63 4/27/2009 6:15:37 PM Copying or circulation without permission are strictly prohibited. This chapter is included in Kringelbach ML and Berridge KC, "Pleasures of the Brain" (c) 2010. Oxford University Press: New York. 64 Pleasures of the Brain medial shell of the nucleus accumbens (sometimes In terms of its neuroanatomical connections, the called ventral striatum) and the ventral pallidum. In ventral pallidum receives convergent signals from the the ventral pallidum particularly, Kyle Smith, in his nucleus accumbens, a brain structure that is implicated doctoral dissertation work in our laboratories, identi- generally in rewards (see Figure 3.1) (Baldo and Kelley, G ed a 0.8 mm3 hedonic hotspot in the posterior end of 2007; Burke et al., Chapter 2, this book; Carelli and ventral pallidum in rats (Smith et al., Chapter 1, this Wightman, 2004; Day and Carelli, 2007; Garris and book). If hotspots are scaled to overall brain size, the Rebec, 2002; Knutson et al., 2001a; Kringelbach, volume of a corresponding hotspot in humans might Chapter 12, this book; Leknes and Tracey, Chapter 19, be closer to a cubic centimeter. In the ventral pallidum this book; Salamone et al., 2007; Schultz, 2006; Smith hotspot, for example, opioid stimulation caused over a et al., Chapter 1, this book; Wan and Peoples, 2006). doubling in the level of ‘liking’ reactions elicited by Ventral pallidum also receives signals from other key sucrose taste (Smith and Berridge, 2005; Tindell et al., limbic structures in the forebrain such as amygdala, 2006). orbitofrontal cortex, and insular cortex, as well as Another reason to focus on ventral pallidum for inputs from reward-related structures in the brainstem sensory pleasures is that electrophysiological record- such as ventral tegmentum and parabrachial nucleus ings of neurons in its same hotspot, by Amy Tindell (Groenewegen and Trimble, 2007; Heimer and Van in her own dissertation study in the Aldridge labora- Hoesen, 2006; Kalivas and Volkow, 2005; Zahm, tory, revealed vigorous G ring in response to the taste 2006). In return, the ventral pallidum sends output of sugar (Tindell et al., 2004). With learning, ventral signals back to limbic areas of prefrontal cortex via the pallidal neurons shifted their activation pattern grad- dorsomedial thalamus (Figure 3.1), including orbitof- ually to G re in response to predictive cues that were rontal, anterior cingulate, and insular regions of cor- associated with sweet reward.
Load more

Recommended publications
  • Neural Coding and the Statistical Modeling of Neuronal Responses By
    Neural coding and the statistical modeling of neuronal responses by Jonathan Pillow A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Center for Neural Science New York University Jan 2005 Eero P. Simoncelli TABLE OF CONTENTS LIST OF FIGURES v INTRODUCTION 1 1 Characterization of macaque retinal ganglion cell responses using spike-triggered covariance 5 1.1NeuralCharacterization.................... 9 1.2One-DimensionalModelsandtheSTA............ 12 1.3Multi-DimensionalModelsandSTCAnalysis........ 16 1.4 Separability and Subspace STC ................ 21 1.5 Subunit model . ....................... 23 1.6ModelValidation........................ 25 1.7Methods............................. 28 2 Estimation of a Deterministic IF model 37 2.1Leakyintegrate-and-firemodel................. 40 2.2Simulationresultsandcomparison............... 41 ii 2.3Recoveringthelinearkernel.................. 42 2.4Recoveringakernelfromneuraldata............. 44 2.5Discussion............................ 46 3 Estimation of a Stochastic, Recurrent IF model 48 3.1TheModel............................ 52 3.2TheEstimationProblem.................... 54 3.3ComputationalMethodsandNumericalResults....... 57 3.4TimeRescaling......................... 60 3.5Extensions............................ 61 3.5.1 Interneuronalinteractions............... 62 3.5.2 Nonlinear input ..................... 63 3.6Discussion............................ 64 AppendixA:ProofofLog-ConcavityofModelLikelihood..... 65 AppendixB:ComputingtheLikelihoodGradient........
    [Show full text]
  • Neural Oscillations As a Signature of Efficient Coding in the Presence of Synaptic Delays Matthew Chalk1*, Boris Gutkin2,3, Sophie Dene` Ve2
    RESEARCH ARTICLE Neural oscillations as a signature of efficient coding in the presence of synaptic delays Matthew Chalk1*, Boris Gutkin2,3, Sophie Dene` ve2 1Institute of Science and Technology Austria, Klosterneuburg, Austria; 2E´ cole Normale Supe´rieure, Paris, France; 3Center for Cognition and Decision Making, National Research University Higher School of Economics, Moscow, Russia Abstract Cortical networks exhibit ’global oscillations’, in which neural spike times are entrained to an underlying oscillatory rhythm, but where individual neurons fire irregularly, on only a fraction of cycles. While the network dynamics underlying global oscillations have been well characterised, their function is debated. Here, we show that such global oscillations are a direct consequence of optimal efficient coding in spiking networks with synaptic delays and noise. To avoid firing unnecessary spikes, neurons need to share information about the network state. Ideally, membrane potentials should be strongly correlated and reflect a ’prediction error’ while the spikes themselves are uncorrelated and occur rarely. We show that the most efficient representation is when: (i) spike times are entrained to a global Gamma rhythm (implying a consistent representation of the error); but (ii) few neurons fire on each cycle (implying high efficiency), while (iii) excitation and inhibition are tightly balanced. This suggests that cortical networks exhibiting such dynamics are tuned to achieve a maximally efficient population code. DOI: 10.7554/eLife.13824.001 *For correspondence: Introduction [email protected] Oscillations are a prominent feature of cortical activity. In sensory areas, one typically observes Competing interests: The ’global oscillations’ in the gamma-band range (30–80 Hz), alongside single neuron responses that authors declare that no are irregular and sparse (Buzsa´ki and Wang, 2012; Yu and Ferster, 2010).
    [Show full text]
  • An Optogenetic Approach to Understanding the Neural Circuits of Fear Joshua P
    Controlling the Elements: An Optogenetic Approach to Understanding the Neural Circuits of Fear Joshua P. Johansen, Steffen B.E. Wolff, Andreas Lüthi, and Joseph E. LeDoux Neural circuits underlie our ability to interact in the world and to learn adaptively from experience. Understanding neural circuits and how circuit structure gives rise to neural firing patterns or computations is fundamental to our understanding of human experience and behavior. Fear conditioning is a powerful model system in which to study neural circuits and information processing and relate them to learning and behavior. Until recently, technological limitations have made it difficult to study the causal role of specific circuit elements during fear conditioning. However, newly developed optogenetic tools allow researchers to manipulate individual circuit components such as anatom- ically or molecularly defined cell populations, with high temporal precision. Applying these tools to the study of fear conditioning to control specific neural subpopulations in the fear circuit will facilitate a causal analysis of the role of these circuit elements in fear learning and memory. By combining this approach with in vivo electrophysiological recordings in awake, behaving animals, it will also be possible to determine the functional contribution of specific cell populations to neural processing in the fear circuit. As a result, the application of optogenetics to fear conditioning could shed light on how specific circuit elements contribute to neural coding and to fear learning and memory. Furthermore, this approach may reveal general rules for how circuit structure and neural coding within circuits gives rise to sensory experience and behavior. Key Words: Electrophysiology, fear conditioning, learning and circuits and the identification of sites of neural plasticity in these memory, neural circuits, neural plasticity, optogenetics circuits.
    [Show full text]
  • 6 Optogenetic Actuation, Inhibition, Modulation and Readout for Neuronal Networks Generating Behavior in the Nematode Caenorhabditis Elegans
    Mario de Bono, William R. Schafer, Alexander Gottschalk 6 Optogenetic actuation, inhibition, modulation and readout for neuronal networks generating behavior in the nematode Caenorhabditis elegans 6.1 Introduction – the nematode as a genetic model in systems neurosciencesystems neuroscience Elucidating the mechanisms by which nervous systems process information and gen- erate behavior is among the fundamental problems of biology. The complexity of our brain and plasticity of our behaviors make it challenging to understand even simple human actions in terms of molecular mechanisms and neural activity. However the molecular machines and operational features of our neural circuits are often found in invertebrates, so that studying flies and worms provides an effective way to gain insights into our nervous system. Caenorhabditis elegans offers special opportunities to study behavior. Each of the 302 neurons in its nervous system can be identified and imaged in live animals [1, 2], and manipulated transgenically using specific promoters or promoter combinations [3, 4, 5, 6]. The chemical synapses and gap junctions made by every neuron are known from electron micrograph reconstruction [1]. Importantly, forward genetics can be used to identify molecules that modulate C. elegans’ behavior. Forward genetic dis- section of behavior is powerful because it requires no prior knowledge. It allows mol- ecules to be identified regardless of in vivo concentration, and focuses attention on genes that are functionally important. The identity and expression patterns of these molecules then provide entry points to study the molecular mechanisms and neural circuits controlling the behavior. Genetics does not provide the temporal resolution required to study neural circuit function directly.
    [Show full text]
  • Exploring the Function of Neural Oscillations in Early Sensory Systems
    FOCUSED REVIEW published: 15 May 2010 doi: 10.3389/neuro.01.010.2010 Exploring the function of neural oscillations in early sensory systems Kilian Koepsell1*, Xin Wang 2, Judith A. Hirsch 2 and Friedrich T. Sommer1* 1 Redwood Center for Theoretical Neuroscience, University of California, Berkeley, CA, USA 2 Neuroscience Graduate Program, University of Southern California, Los Angeles, CA, USA Neuronal oscillations appear throughout the nervous system, in structures as diverse as the cerebral cortex, hippocampus, subcortical nuclei and sense organs. Whether neural rhythms contribute to normal function, are merely epiphenomena, or even interfere with physiological processing are topics of vigorous debate. Sensory pathways are ideal for investigation of oscillatory activity because their inputs can be defined. Thus, we will focus on sensory systems Edited by: S. Murray Sherman, as we ask how neural oscillations arise and how they might encode information about the University of Chicago, USA stimulus. We will highlight recent work in the early visual pathway that shows how oscillations Reviewed by: can multiplex different types of signals to increase the amount of information that spike trains Michael J. Friedlander, Baylor College of Medicine, USA encode and transmit. Last, we will describe oscillation-based models of visual processing and Jose-Manuel Alonso, Sociedad Espanola explore how they might guide further research. de Neurociencia, Spain; University of Connecticut, USA; State University Keywords: LGN, retina, visual coding, oscillations, multiplexing of New York, USA Naoum P. Issa, University of Chicago, USA NEURAL OSCILLATIONS IN EARLY However, the autocorrelograms are subject to *Correspondence: SENSORY SYSTEMS confounds caused by the refractory period and Oscillatory neural activity has been observed spectral peaks often fail to reveal weak rhythms.
    [Show full text]
  • A Barrel of Spikes Reach out and Touch
    HIGHLIGHTS NEUROANATOMY Reach out and touch Dendritic spines are a popular sub- boutons (where synapses are formed ject these days. One theory is that on the shaft of the axon) would occur they exist, at least in part, to allow when dendritic spines were able to axons to synapse with dendrites bridge the gap between dendrite and without deviating from a nice axon. They carried out a detailed straight path through the brain. But, morphological study of spiny neuron as Anderson and Martin point out in axons in cat cortex to test this Nature Neuroscience, axons can also hypothesis. form spine-like structures, known as Perhaps surprisingly, they found terminaux boutons. Might these also that the two types of synaptic bouton be used to maintain economic, did not differentiate between den- straight axonal trajectories? dritic spines and shafts. Axons were Anderson and Martin proposed just as likely to use terminaux boutons that, if this were the case, the two to contact dendritic spines as they types of axonal connection — were to use en passant boutons, even terminaux boutons and en passant in cases where it would seem that the boutons — would each make path of the axon would allow it to use synapses preferentially with different an en passant bouton. So, why do types of dendritic site. Terminaux axons bother to construct these deli- boutons would be used to ‘reach out’ cate structures, if not simply to con- to dendritic shafts, whereas en passant nect to out-of-the-way dendrites? NEURAL CODING exploring an environment, a rat will use its whiskers to collect information by sweeping them backwards and forwards, and it could use a copy of the motor command to predict A barrel of spikes when the stimulus was likely to have occurred.
    [Show full text]
  • Neural Coding Computation and Dynamics
    Neural Coding Computation and Dynamics September 15–18, 2007 Sporting Casino Hossegor 119, avenue Maurice Martin Hossegor, France Programme Summary Saturday, September 15 18:30 – 20:00 Reception 20:00 – 22:00 Dinner Sunday, September 16 10:00 – 11:15 Talks: Ganguli, Ratcliff . 7, 11 11:15 – 11:45 Break 11:45 – 13:00 Talks: Beck, Averbeck . 6, 5 13:15 – 14:30 Lunch 15:30 – 17:30 Posters 17:30 – 18:15 Talks: Kass ..................................... 8 18:15 – 18:45 Break 18:45 – 19:45 Talks: Staude, Roxin . 15, 11 20:00 – 22:00 Dinner Monday, September 17 10:00 – 11:15 Talks: Smith, H¨ausler . 13, 8 11:15 – 11:45 Break 11:45 – 13:00 Talks: Thiele, Tolias . 16, 16 13:15 – 14:30 Lunch 15:30 – 17:30 Posters 17:30 – 18:15 Talks: Nirenberg . 10 18:15 – 18:45 Break 18:45 – 19:45 Talks: Shlens, Kretzberg . 13, 9 20:00 – 22:00 Dinner Tuesday, September 18 10:00 – 11:15 Talks: Shenoy, Solla . 12, 14 11:15 – 11:45 Break 11:45 – 13:00 Talks: Harris, Machens . 7, 9 13:15 – 14:30 Lunch 14:30 – 15:15 Talks: O’Keefe . 10 15:15 – 15:45 Break 15:45 – 16:45 Talks: Siapas, Frank . 13, 6 ii NCCD 07 Programme Saturday – Sunday Programme Saturday, September 15 Evening 18:30 – 20:00 Reception 20:00 – 22:00 Dinner Sunday, September 16 Morning 10:00 – 10:45 Spikes, synapses, learning and memory in simple networks Surya Ganguli, University of California, San Francisco . 7 10:45 – 11:15 Modeling behavioural reaction time (RT) data and neural firing rates Roger Ratcliff, Ohio State University .
    [Show full text]
  • Neurophysiological and Computational Principles of Cortical Rhythms in Cognition
    Physiol Rev 90: 1195–1268, 2010; doi:10.1152/physrev.00035.2008. Neurophysiological and Computational Principles of Cortical Rhythms in Cognition XIAO-JING WANG Department of Neurobiology and Kavli Institute of Neuroscience, Yale University School of Medicine, New Haven, Connecticut I. Introduction 1196 A. Synchronization and stochastic neuronal activity in the cerebral cortex 1196 B. Cortical oscillations associated with cognitive behaviors 1197 C. Interplay between neuronal and synaptic dynamics 1199 D. Organization of this review 1200 II. Single Neurons as Building Blocks of Network Oscillations 1200 A. Phase-response properties of type I and type II neurons 1201 B. Resonance 1203 C. Subthreshold and mixed-mode membrane oscillations 1204 D. Rhythmic bursting 1206 III. Basic Mechanisms for Network Synchronization 1207 A. Mutual excitation between pyramidal neurons 1207 B. Inhibitory interneuronal network 1208 C. Excitatory-inhibitory feedback loop 1209 D. Synaptic filtering 1211 E. Slow negative feedback 1211 F. Electrical coupling 1212 G. Correlation-induced stochastic synchrony 1213 IV. Network Architecture 1213 A. All-to-all networks: synchrony, asynchrony, and clustering 1214 B. Sparse random networks 1214 C. Complex networks 1214 D. Spatially structured networks: propagating waves 1217 E. Interaction between diverse cell types 1219 F. Interaction across multiple network modules 1219 V. Synchronous Rhythms With Irregular Neural Activity 1222 A. Local field oscillations versus stochastic spike discharges of single cells 1222 B. Sparsely synchronized oscillations 1224 C. Specific cases: fast cortical rhythms 1227 VI. Functional Implications: Synchronization and Long-Distance Communication 1229 A. Methodological considerations 1229 B. Phase coding 1232 C. Learning and memory 1235 D. Multisensory integration 1236 E.
    [Show full text]
  • Introduction to Spiking Neural Networks: Information Processing, Learning and Applications
    Review Acta Neurobiol Exp 2011, 71: 409–433 Introduction to spiking neural networks: Information processing, learning and applications Filip Ponulak1,2* and Andrzej Kasiński1 1Institute of Control and Information Engineering, Poznan University of Technology, Poznan, Poland, *Email: [email protected]; 2Princeton Neuroscience Institute and Department of Molecular Biology, Princeton University, Princeton, USA The concept that neural information is encoded in the firing rate of neurons has been the dominant paradigm in neurobiology for many years. This paradigm has also been adopted by the theory of artificial neural networks. Recent physiological experiments demonstrate, however, that in many parts of the nervous system, neural code is founded on the timing of individual action potentials. This finding has given rise to the emergence of a new class of neural models, called spiking neural networks. In this paper we summarize basic properties of spiking neurons and spiking networks. Our focus is, specifically, on models of spike-based information coding, synaptic plasticity and learning. We also survey real-life applications of spiking models. The paper is meant to be an introduction to spiking neural networks for scientists from various disciplines interested in spike-based neural processing. Key words: neural code, neural information processing, reinforcement learning, spiking neural networks, supervised learning, synaptic plasticity, unsupervised learning INTRODUCTION gates (Maass 1997). Due to all these reasons SNN are the subject of constantly growing interest of scientists. Spiking neural networks (SNN) represent a special In this paper we introduce and discuss basic con- class of artificial neural networks (ANN), where neu- cepts related to the theory of spiking neuron models.
    [Show full text]
  • Neural Coding in Barrel Cortex During Whisker-Guided Locomotion 1
    1 TITLE: Neural coding in barrel cortex during whisker-guided locomotion 2 3 Sofroniew, NJ 1, #, Vlasov, YA 1,2, #, Hires, SA 1, 3, Freeman, J 1, Svoboda, K 1 4 5 1 Janelia Research Campus, Ashburn VA 20147, USA 6 7 2 IBM T. J. Watson Research Center, Yorktown Heights, New York 10598, USA 8 9 3 Current address: Biological Sciences, University of Southern California, Los Angeles, 10 CA, USA 11 # These authors contributed equally to this work 12 13 ABSTRACT 14 15 Animals seek out relevant information by moving through a dynamic world, but sensory 16 systems are usually studied under highly constrained and passive conditions that may not 17 probe important dimensions of the neural code. Here we explored neural coding in the 18 barrel cortex of head-fixed mice that tracked walls with their whiskers in tactile virtual 19 reality. Optogenetic manipulations revealed that barrel cortex plays a role in wall- 20 tracking. Closed-loop optogenetic control of layer 4 neurons can substitute for whisker- 21 object contact to guide behavior resembling wall tracking. We measured neural activity 22 using two-photon calcium imaging and extracellular recordings. Neurons were tuned to 23 the distance between the animal snout and the contralateral wall, with monotonic, 24 unimodal, and multimodal tuning curves. This rich representation of object location in the 25 barrel cortex could not be predicted based on simple stimulus-response relationships 26 involving individual whiskers and likely emerges within cortical circuits. 27 28 INTRODUCTION 29 Animals must understand the spatial relationships of objects in their environment for 30 navigation.
    [Show full text]
  • Temporal Coding of Sensory Information in the Brain
    Acoust. Sci. & Tech. 22, 2 (2001) TUTORIAL Temporal coding of sensory information in the brain Peter A. Cariani Department of Otology and Laryngology, Harvard Medical School, Eaton Peabody Laboratory, Massachusetts Eye & Ear Infirmary, 243 Charles St., Boston, MA 02114 USA e-mail: [email protected] Abstract: Physiological and psychophysical evidence for temporal coding of sensory qualities in dif- ferent modalities is considered. A space of pulse codes is outlined that includes 1) channel-codes (across-neural activation patterns), 2) temporal pattern codes (spike patterns), and 3) spike latency codes (relative spike timings). Temporal codes are codes in which spike timings (rather than spike counts) are critical to informational function. Stimulus-dependent temporal patterning of neural responses can arise extrinsically or intrinsically: through stimulus-driven temporal correlations (phase-locking), re- sponse latencies, or characteristic timecourses of activation. Phase-locking is abundant in audition, mechanoception, electroception, proprioception, and vision. In phase-locked systems, temporal differ- ences between sensory surfaces can subserve representations of location, motion, and spatial form that can be analyzed via temporal cross-correlation operations. To phase-locking limits, patterns of all-order interspike intervals that are produced reflect stimulus autocorrelation functions that can subserve rep- resentations of form. Stimulus-dependent intrinsic temporal response structure is found in all sensory systems. Characteristic temporal patterns that may encode stimulus qualities can be found in the chem- ical senses, the cutaneous senses, and some aspects of vision. In some modalities (audition, gustation, color vision, mechanoception, nocioception), particular temporal patterns of electrical stimulation elicit specific sensory qualities. Keywords: Temporal coding, Phase-locking, Autocorrelation, Interspike interval, Spike latency, Neu- rocomputation PACS number: 43.10.Ln, 43.64.Bt, 43.66.Ba, 43.66.Hg, 43.66.Wv 1.
    [Show full text]
  • Is Coding a Relevant Metaphor for the Brain?
    bioRxiv preprint doi: https://doi.org/10.1101/168237; this version posted July 13, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Is coding a relevant metaphor for the brain? Romain Brette1* 1 Sorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Institut de la Vision, 17 rue Moreau, 75012 Paris, France * Correspondence: R. Brette, Institut de la Vision, 17, rue Moreau, 75012 Paris, France [email protected] http://romainbrette.fr Short abstract I argue that the popular neural coding metaphor is often misleading. First, the “neural code” often spans both the experimental apparatus and the brain. Second, a neural code is information only by reference to something with a known meaning, which is not the kind of information relevant for a perceptual system. Third, the causal structure of neural codes (linear, atemporal) is incongruent with the causal structure of the brain (circular, dynamic). I conclude that a causal description of the brain cannot be based on neural codes, because spikes are more like actions than hieroglyphs. Long abstract “Neural coding” is a popular metaphor in neuroscience, where objective properties of the world are communicated to the brain in the form of spikes. Here I argue that this metaphor is often inappropriate and misleading. First, when neurons are said to encode experimental parameters, the neural code depends on experimental details that are not carried by the coding variable.
    [Show full text]