What psychological process mediates feeding evoked by electrical stimulation of the lateral hypothalamus?

“" (Berridge and Valenstein 1991, p. 9) and " In other words, dopamine systems are necessary for 'wanting' incentives, but not for 'liking' them or for learning new 'likes' and 'dislikes' (Berridge and Robinson 1998, p. 309).”

“My colleagues and I have suggested that the primary motivational role of such systems is to attribute incentive salience to selected percepts and representations (13,15,16,106).”

“However, contrary to that tastier food hypothesis, Berridge and Valenstein found that LH stimulation failed to enhance ''liking'' reactions to sweetness, even though it made the rats ''want'' to eat at least four times more than normal amounts (Berridge and Valenstein, 1991).”

“…established dissociations between the apparent incentive value of drugs (and natural rewards, such as food), and their ability to engender pleasure, that we suggested a distinction be made between “wanting” and liking” (Berridge & Valenstein, 1991; Robinson & Berridge, 1993; Berridge, 1996).”

“The incentive salience model was proposed around 1990 as a way to reconcile why brain dopamine sometimes seemed to mediate sensory pleasure, when it actually does not [15,16].”

“However, the same electrodes that make rats 'want' to eat food more voraciously still fail to make rats 'like' food more hedonically (Berridge and Valenstein 1991).”

“Our first discovery of enhanced 'wanting'-without-'liking' came two decades ago from a study on eating evoked by electrical stimulation of the lateral hypothalamus in rats, conducted collaboratively with Elliot Valenstein (Berridge and Valenstein, 1991).”

“…suggests that accumbens dopamine neurotransmission modulates the attribution of incentive salience to reward cues, which triggers a motivational state of “wanting” for both the cue and its associated reward (Berridge and Valenstein, 1991; Robinson and Berridge, 1993; Berridge and Robinson, 1998).”

“It was noted that, at least with regard to the magnitude and immediacy of the effect, hyperphagia induced by functional inhibition of the Acb shell strongly resembled stimulus-bound feeding seen in studies of lateral hypothalamic (LH) electrical stimulation [30] or in experiments using local infusions of glutamate rec…”

“dopamine in particular, my colleagues and I have called this process ‘ incentive salience ’, and have attempted to define some of its properties [11,12,118,119,131,132].”

“Electrical brain stimulation of mesocorticolimbic circuitry may also elicit quite broad ‘wanting’ of many targets, especially initially (Valenstein, 1971; Berridge & Valenstein, 1991; Heath, 1996; Kringelbach et al., 2010).”

“Observation of increased eating without enhanced hedonic impact appears somewhat similar to dissociations of food “wanting” from “liking” produced by other manipulations of mesolimbic function (Berridge and Valenstein, 1991; Reynolds and Berridge, 2002; Wyvell and Berridge, 2000; Peciña et al., 2003).”

“Our results are reminiscent of similar reports of increased wanting accompanied by slightly decreased “liking” produced by amphetamine microinjection in the nucleus accumbens and by electrical stimulation of the medial forebrain bundle (Berridge and Valenstein, 1991; Wyvell and Berridge, 2000).”

“Enhancement of eating by NAc opioid stimulation is well-known (1, 31, 35, 53), and eating enhancement by NAc amphetamine, although more fragile, is also consistent with prior reports (67, 68) as well as our hypothesis that dopamine mediates incentive salience in a manner sufficient to drive motivated behavior like eat…”

“Incentive salience attribution was hypothesized to be linked directly to activation of the mesocorticolimbic dopamine system (Berridge and Valenstein, 1991).”

“Instead, mesolimbic electrodes may have generally produced a false pleasure, that is, by generating motivational ‘wanting’ without hedonic ‘liking’ (Berridge and Valenstein 1991; Berridge 2003).”

“…normal appetite, which if attributed to neural representations of reward cues causes both the cues and associated Pavlovian rewards themselves to become attractive and “wanted,” triggering approach and pursuit behaviors (Berridge and Valenstein, 1991; Berridge and Robinson, 1998; Berridge, 2001).”

“…example, Berridge and colleagues suggest that incentive salience is attributed by mesoaccumbens systems to neural representations of food, drugs, or other reward-related stimuli (Berridge and Valenstein, 1991; Robinson and Berridge, 1993; Berridge and Robinson, 1998; Wyvell and Berridge, 2000 ).”

“This distinction might be related to the “wanting” without “liking” evoked by dopamine and GABA manipulations in nucleus accumbens, which appear to be mediated by motivational incentive salience mechanisms that are separable from hedonic impact mechanisms (Berridge and Valenstein, 1991; Wyvell and Berridge, 2000; Reyn…”

“…rapid onset, and general profile of feeding following medial accumbens DNQX infusions bore a striking resemblance to the ingestive behavior observed following electrical stimulation of the lateral hypothalamus (Valenstein , 1969; Wise, 1974; Stellar et al., 1979; Berridge and Valenstein , 1991).”

“…pure indication of affect because they can be isolated from the sensory properties of a taste (see Berridge, 2000), they can be dissociated from the desire to eat (e.g. Berridge & Valenstein, 1991; Berridge et al. 1989) and they often correspond to human subjective ratings of palatability.”

“Using this measure of taste hedonic impact, Berridge and Valenstein (1991) found that electrical stimulation of LH completely failed to enhance positive hedonic reactions to sucrose, despite making the rats eat over four times as much food.”

“However, wanting and liking can be dissociated (Berridge & Valenstein, 1991; Robinson & Berridge, 1993, 2003), with dopamine being involved in wanting rather than liking.”

“…"wanting" separate dramatically, and we have therefore proposed that the Bindra-Toates model of incentive motivation be modified to allow separate control of these two incentive processes (Berridge, 1996; Berridge & Valenstein , 1991; Berridge, Venier, & Robinson, 1989; Robinson & Berridge, 1993).”

“Some animal research has suggested that the state of wanting involves aversive facial expressions (e.g., Berridge and Valenstein 1991), but the evidence is still not conclusive.”

“…were said to reveal prepotent behaviors, which became progressively stamped in, such that their performance during electrical stimulation increased dramatically (in part due to activation of the medial forebrain bundle that passes through the lateral hypothalamus) (Berridge and Valenstein, 1991).”

“The TD error d was identified with the ‘‘reboosting’’ process of a CS posited by the incentive salience hypothesis to occur at the moment of UCS [1,46].”

“, 1990; Damsma et al., 1992). It is evident, therefore, that with feeding, drinking, and sexual behavior maximal increases in DA release in the NAc occur during consummatory behaviors and much smaller (if any) increases occur during anticipatory behaviors. The results of these microdialysis studies stand in contrast t…”

“Reboosting is posited to be a trial-by-trial restoration of magnified incentive value attributed to the memory representation of conditioned stimuli that occurs when expected reward is actually obtained ( Berridge & Valenstein, 1991; Berridge & Robinson, 1998; Robinson et al., 2005).”

“The lateral hypothalamus is also involved in wanting as electrical stimulation of this area induces rats to vigorously self-stimulate and eat (want) food, although it does not make them like the food more [5].”

“For example, without altering hedonic reactions, the propensity to ingest can be increased by electrical stimulation of the lateral hypothalamus (Berridge & Valenstein, 1991) or reduced by depletion of brain dopamine projections (Berridge et al., 1989).”

“…late 1980s and beginning of the 1990s Kent Berridge and Terry Robinson set the stage for an important turn in hedonia research by proposing to divide reward into the subcomponents of wanting, liking, and learning (Berridge et al., 1989; Berridge and Valenstein, 1991; Robinson and Berridge, 1993).”

“Berridge et al., 1989; Berridge & Valenstein, 1991; Wyvell & Berridge, 2000).”

“An animal study demonstrated that the NAcc of a rat was activated by drugs such as cocaine but its facial affective expression in response to the drugs was a disliking reaction (Berridge and Valenstein, 1991).”

“This reduced motivation may correspond to what Berridge and his colleagues (Berridge and Valenstein 1991; Robinson and Berridge 1993; Berridge 1996) refer to as wanting , as distinct from liking , which is more closely related to alternative hedonic processes.”

“An electrode site that elicits feeding can, depending on stimuli available in the environment, be made to elicit other behaviors, or it may even elicit oral signs of aversion [47].”

“This area is involved in reinforcement (Berridge and Valenstein, 1991; Wise, 1996) and is interconnected with the major hypothalamic nuclei (ie, ARC and PVN) implicated in the metabolic sensing (Kalra and Kalra, 2004) and with the brainstem nuclei, mediating eating-related motor function and…”

“…relevance here are models of the effort exerted to obtain rewards [e.g., by measuring how eagerly the animal runs for rewards in a runway (Berridge and Valenstein, 1991; Peciña et al., 2003) or its willingness to exert effort in exchange for more palatable food rewards (Salamone et al.,…”

“Although these manipulations produce dramatic changes in free intake, they fail to produce a shift in hedonic/aversive palatability as assessed by taste reactivity patterns (11,12,64).”

“Although the reported clinical studies did not differentiate between the different aspects of reward processing deficits that are often indiscriminately measured in humans, ICSS of the lateral hypothalamus of rats, which mediates motivated behaviors (48,49), suggests that antidepressant efficacy may be associated”

“Con-ceptualizinglevelsofvalencemayfocusresearchattentiononthe Shuman et al.”

“Electrical stimulation of sites within the lateral hypothalamic area stimulates feeding [41,275], but it is now well established that neuronal activities in this area represent reward value[243], and psychophysiological experiments suggest that lateral hypothalamic stimulation induces feeding behavior by potentiating…”

“Indeed, wanting can occur even when the hedonic experience is aversive; electrical stimulation in the lateral hypothalamus causes increased intake alongside disliking reactions to sucrose in rats (28).”

“But by contrast to opioid microinjections that induce both 'liking' and 'wanting' for rewards, deep brain electrode stimulation that makes rats eat more nonetheless fails to increase 'liking' reactions to sweetness (Berridge & Valenstein, 1991).”

“, 6-OHDA and amygdala lesions (13,43,81), and by electrical stimulation of the hypothalamus (12).”

“PHARMACOL BIOCHEM BEHAV 46(3) 745-749, 1993.”

“The results are also consistent with microdialysis studies of accumbens dopamine (Blackburn and Phillips 1989; Phillips et al. 1991), and with many incentive effects, such as feeding in rats induced by electrical stimulation of the lateral hypothalamus (ESLH) and the induction of cravings in humans by cues associated…”

“Similarly, implanted electrodes to stimulate the mesolimbic systems and elevate extracellular dopamine enhanced ‘wanting’ but not ‘liking’ (Berridge and Valenstein 1991; Berridge and Kringelbach 2015).”

“Here is a recent triumph of science: the creation of vice in rats. Berridge and Valenstein (1991)”

“Soon, however, we also found positive evidence that stimulation of mesolimbic dopamine systems in rats increased their motivational “wanting” to pursue or consume food rewards yet failed to enhance their “liking” of those same rewards (Berridge & Valenstein 1991, Wyvell & Berridge 2000).”

“…rat, the forebrain, including GC, is a part of palatability-related decisionmaking circuitry (Sasamoto et al., 1990; Zhang and Sasamoto, 1990; Berridge and Valenstein, 1991; Kiefer and Orr, 1992; Shammah-Lagnado et al., 1992; Travers et al., 1997; Schafe and Bernstein, 1998; Stehberg et al.,…”

“Hence, alleles of the COMT gene that produce a less efficient COMT enzyme create a situation in which dopamine and norepinephrine remain in the synapse for a longer time (Bilder, Volavka, Lachman, & Grace, 2004).”

“However, a consistent corpus of studies conducted on rodents (Berridge & Valenstein, 1991; Peciña, Cagniard,Berridge, Aldridge, &Zhuang, 2003) has demonstrated that consuming more does not always imply liking more.”

“Berridge and Valenstein (Berridge and Valenstein, 1991) reported that electrical stimulation of the LH increased feeding behavior and also enhanced aversive taste reactions in rats.”

“Conversely, electrical stimulation of the lateral hypothalamus keeps reward-seeking behaviours intact, but these animals exhibit negative hedonic facial reactions when they consume a reward [27].”

“In contrast, “wanting” without “liking” is observed during electrical stimulation of the lateral hypothalamus in rats, which increases feeding behaviors but triggers more aversive facial reactions to various tastes (Berridge & Valenstein, 1991).”

“It is well established that the hypothalamus is critical in the control of food intake (wanting) and energy balance (Berridge and Valenstein, 1991; Berthoud, 2007).”

“1993; Berridge 1996), electrical stimulation (Berridge and Valenstein 1991) and cooling (Berridge and Zajonc 1991) of dopamine system related structures.”

“…neurotransmitter responsible for pleasure, this has since been disproved, and a large body of evidence suggests that it instead modulates Bwanting^ (Berridge & Valenstein, 1991; Peciña, Cagniard, Berridge, Aldridge, & Zhuang, 2003; Tindell, Berridge, Zhang, Peciña, & Aldridge, 2005; Wyvell &…”

“…LH leads to hypophagia (Anand and Brobeck, 1951; Grossman et al., 1978); electrical stimulation of LH drives both voracious eating (Hoebel and Teitelbaum, 1962; Margules and Olds, 1962) and production of orofacial behaviors typically associated with aversive tastes (Berridge and Valenstein, 1991).”

“However, others have suggested LHA stimulation may actually produce a subjective state of craving rather than pleasure per se (Berridge and Valenstein, 1991).”

“Because of a failure to find that activation of “The Brain Reward System” fails to promote (indeed inhibits) positive hedonic facial action patterns (Berridge and Valenstein, 1991), Berridge (2004) chose to call the neural substrate the wanting system, which is a reasonable secondary-process…”