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.