Neurobiology of Sensation and Reward PDF

Preface

A TOAST: TO MAKING SENSATIONS MORE REWARDING

AND REWARDS MORE SENSATIONAL

The Neurobiology of Sensation and Reward provides a comprehensive systems overview of sensory and reward processing in the brain. Although the topics of sensation and reward are critically intertwined at the most fundamental levels of animal behavior, they rarely receive double billing. In the fi eld of contemporary neuroscience, the researchers who study sensation rarely consider the rewards these sensations evoke, and the researchers who study reward tend to ignore the sensations evoking these rewards. Over the last 70 years, beginning perhaps with the rise of Skinnerian behaviorism, the scientifi c treatment of sensation and reward has increasingly diverged. Particularly by the 1950s, when intracranial electrical and drug self-stimulation techniques came into vogue, the behavioral and neural bases of reward could be studied entirely in the absence of environmental (sensory) input. The role of the sensory stimulus became relegated to second-best.

In 2011, this rather arbitrary and counterproductive dualism continues to dominate the neuroscience landscape. For example, despite the wealth of exciting new information regarding reward learning in the brain, surprisingly little is said about how the sensory specifi city of reward processing is even achieved. Surely the functional integrity of a reward system is only as secure as its driving sensory inputs. Thus, a synthesis is in order, and this book is the fi rst attempt to reunite these drifting neuro-tectonic plates by highlighting the important and intimate links between sensation and reward. In examining the neurobiological interface between sensation and reward, the book will reveal how the intrinsic properties of sensory systems effectively defi ne and constrain the ambitions of reward-related processing in human and non-human brains. What can reward processing teach us about the senses, and what can sensory processing teach us about reward?

Once upon a time, say 500 million years ago, sensations and rewards clearly occupied the same ecological niche. All detectable sensations promised or exemplifi ed reward; in turn, all rewards were necessarily embodiments of sensory stimuli. (This is not to minimize the importance of unrewarding sensations, but the topic of aversive stimuli is reserved for another book.) Indeed, insofar as rewards are those things that promote (reinforce) behavior, any sensory detector unable to provide biologically adaptive (i.e., rewarding) information for an organism would have soon been traded out of the gene pool, a victim of natural selection. During the phlegmatic era of Precambrian coelenterates, the only utility of sensory detection was to increase the chances of survival, and if a jellyfi sh or hydroid happened to sprout a novel detector apparatus that had no bearing on its fi tness or longevity, this feature would have disappeared under evolutionary pressures.

Yet a curious implication arises out of these considerations: basic reward processing does not actually require a brain, at least not in the cortical sense. If one is willing to accept an operational defi nition of reward as reinforcement, then this suggests that all manner of species are under the spell of rewarding sensory stimuli. Brain or no, any organism that modifi es its behavior to maximize access to a reward should qualify. Humans, monkeys, dogs, rats, obviously; but also coelenterates, cellular slime molds, ciliated protozoa. Each of these species will orient itself, or migrate, toward a food source diffusing through an aqueous medium. Sensory rewards in the general adaptive sense can reinforce behavior of bacteria, viruses, even plants. After all, sunlight will induce phototaxis in a green plant, such that it will extend its shoots and fronds up into the sky. Is the sunlight not thus a kind of sensory "reward" for the plant, operating at an extremely slow timescale?

The preceding discussion raises intriguing questions that will form an important organizational theme of the book. Specifi cally: what distinct advantages does a central nervous system confer upon reward processing in an organism endowed with a brain? In other words, how does the processing of a reward actually benefi t from the presence of a brain? Some possibilities include the ability to integrate information from multiple sensory modalities in the service of reward; the ability to predict and anticipate reward; the ability to defer the consumption of a reward for another time; the ability to select among several rewarding alternatives; the ability to overcome natural (innate) response tendencies elicited by a reward; the ability to assign meaning to a reward. These questions are masterfully considered in the chapter by Murray, Wise, and Rhodes in this volume.

The book is divided into four parts. Each chapter can be read on its own of course, though the full scope of the book is best appreciated as a passage through all chapters in sequence. Part I, "First Principles," sets the tone for the remaining chapters of the volume, and introduces historical, ecological, and evolutionary themes that will recur throughout the book. The opening chapter, by Norman Weinberger and Kasia Bieszczad, presents a forceful case for treating the neurobiology of sensation and reward as a continuum rather than as separate frontiers, and serves as a proximal "bookend" for the volume. In the following chapter, Larry Marks traces a brief, but not too brief, scientifi c history of sensation and reward, beginning with Greek philosophers and Egyptian pharaohs, in an attempt to chart how scientifi c thinking about sensory perception and hedonics has converged and diverged throughout human history. Norman White then provides a scholarly unpacking of the concept of "reward," using his chapter to defi ne rewards and reinforcers, to illustrate why not all rewards are reinforcing and why not all reinforcers are rewarding, and to outline how behavioral paradigms can be used to dissociate among different and competing forms of reward. Finally, as mentioned above, Elisabeth Murray, Steven Wise, and Sarah Rhodes delve deep into the question of how the evolutionary development of the brain confers progressively greater complexity of reward processing, comprehensively spanning the phylogenetic scale from invertebrates to humans.

Part II of the book, "A Systems Organization of the Senses," offers an overview of the fi ve senses. All of the contributing authors in this section—Jay Gottfried and Don Wilson on "Smell," Don Katz and Brian Sadacca on "Taste," Steven Hsiao and Manuel Gomez-Ramirez on "Touch," Christina Konen and Sabine Kastner on "Sight," and Corrie Camalier and Jon Kaas on "Sound"—bring their sensory systems expertise to bear on questions of sensory coding and the implications for reward processing. Because the natural (real-world) form of sensory objects necessarily constrains the type of information that a central nervous system can extract from the environment, these chapters include sensory ecological and evolutionary perspectives as a bridge for understanding how brain systems generate and maintain perceptual codes of meaningful objects that ultimately subserve reward processing. The chapter by Hsiao and Gomez-Ramirez ("Touch") additionally contains a section on multisensory integration, where the important point is made that brain structures traditionally thought to be unisensory are infl uenced by sensory information from other modalities. The fi nal chapter in this section, "Sensory Agnosias," by H. Branch Coslett, focuses on neurobehavioral syndromes associated with higher-order sensory perceptual defi cits, and highlights how patient lesion models can be used to gain a better mechanistic understanding of sensory perception and awareness in the human brain. In order to allay any false hopes that might reasonably arise from a book with the word "Reward" in the title, it should be noted that the sensory chapters do not include dedicated discussions of sensory-specifi c hedonics, valence coding, or neural hot spots of pleasantness, fi rst, because there are many other recent fi ne review articles and books that do just this, and second, because a determination of hedonics in non-human animals relies on indirect measures and can be diffi cult to relate to human models.

Part III of the book, "From Sensation to Reward," serves as a counterpoint to Part II, with chapters that directly consider the interplay between reward systems and the sensory cues that drive them. In the fi rst chapter of this section, Suzanne Haber takes a slightly unique approach in laying out the neuroanatomy of reward. Her starting point is the basal ganglia, and particularly the ventral striatum, a region that is perfectly poised to straddle sensations and rewards, being densely interconnected both with cortical sensory systems and with reward-based systems underlying learning and behavior. Ivan de Araujo follows with a challenge to the doctrine of "sweet taste = primary reward," his point being that there are numerous instantiations of a reward, both proximal and distal, pre-ingestive and post-ingestive, affording multiple opportunities for relating external (sensory) and internal (endocrine, autonomic) cues to neural representations of reward that can variously guide adaptive behavior. The subsequent chapter by Bernard Balleine describes the behavioral neuroscience of incentive learning, an associative learning mechanism that perfectly epitomizes the integration of sensations, rewards, and motivational states to control goal-directed actions. John O'Doherty presents an up-to-date overview of reward prediction. He specifi cally focuses on the different ways that a given (sensory) stimulus can enter into conditioned associations, including Pavlovian, instrumental, and habitual learning, and describes imaging and computational approaches to reveal how different types of learning lead to different representations of predictive reward signals in the brain. Fresh insights into the role of the orbitofrontal cortex in mediating adaptive behavior is the focus of Geoff Schoenbaum, Matthew Roesch, Tom Stalnaker, and Yuji Takahashi, whose chapter contends that this brain region signals predictive information about what the future holds, responding not only to reward, but to reward anticipation and to reward-predicting sensory cues. The last chapter of this section is by Lesley Fellows and complements Coslett's chapter in the prior section. This chapter illustrates the neuropsychological consequences of damage to brain reward systems and puts forward a bold new hypothesis that the decision-making defi cits observed in patients with prefrontal injury underscore a neurology of value.

Part IV, "Civilized Sensory Rewards (Distinctly Human Rewards)," is the coda to the book. The chapter authors in this section have been encouraged to weave empirical data with unbridled speculation, to consider the neurobiology of these higher-order rewarding sensory experiences, and how they might fi t into broader schemas of sensation and reward. Are the "civilized" sensory rewards of perfume, art, and music truly distinct to humans, and if so, why? What rewarding functions do they serve (if any), and by what mechanisms do they accomplish these functions? One could speculate that the sensory information transmitted by attar of roses, the Venus de Milo, or the Moonlight Sonata is hardwired to human reward systems. Or alternatively, perhaps humans are hardwired to create certain types of art objects that specifi cally engage our reward systems. In her chapter on "Perfume," Rachel Herz outlines the history and sociology of perfume and considers the putative roles of fi ne fragrances as human pheromone-like compounds, aphrodisiacs, and reproductive lures. The emotional potency of smells in general is considered in the context of associative learning processes and empirical neuroimaging data, linking back to previous chapters in the book. The chapter by Anjan Chatterjee on "Visual Art" discusses the interface between visual art and the brain, highlighting different levels of visual complexity as represented both in the brain and in art, and he provides a new framework for neuroaesthetics research that may usefully guide hypothesis-driven work on this topic in future. To conclude, Zald and Zatorre ponder in their chapter on "Music" why humans take pleasure from sequences of tones, and they articulate some of the possible mechanisms by which music exerts this effect. They end with the idea that the rewarding aspects of music lie in its ability to anticipate, defer, and confi rm delivery of a known auditory outcome, in keeping with neurobiological models of reward prediction.

In bringing together contributions from leading investigators in the fi elds of sensation and reward, all under a single volume, this book is meant to inject the "sensory" back into the study of reward processing, and the "rewarding" back into the study of sensory processing. It is hoped that the combined perspectives of neurobiology, ecology, and evolution will create interest and enthusiasm for cross-disciplinary scientifi c collaborations that bridge the interface between sensation and reward.