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Amsterdam, J. D., Settle, R. G., Doty, R. L., Abelman, E., and Winokur, A. (1987). Taste and smell perception in depression. Biol. Psychiat. 22, 1481–1485. doi: 10.1016/0006-3223(87)90108-9 In parallel with the initial work that established the dependence of MFB self-stimulation on dopaminergic neurotransmission, detailed psychophysical studies were carried out to characterize the directly stimulated neurons responsible for the rewarding effect ( Gallistel et al., 1981). The estimated characteristics include recovery from refractoriness ( Yeomans, 1975, 1979; Bielajew et al., 1982), conduction velocity ( Shizgal et al., 1980; Bielajew and Shizgal, 1982, 1986; Murray and Shizgal, 1996a, b), frequency following ( Gallistel, 1978; Simmons and Gallistel, 1994; Solomon et al., 2015), and the behaviorally relevant direction of conduction ( Bielajew and Shizgal, 1986). The results are consistent with the hypothesis that the principal constituents of the directly activated substrate for MFB self-stimulation are neurons with descending myelinated axons. In contrast, the dopaminergic fibers in the rat MFB have slow-conducting ( Feltz and Albe-Fessard, 1972; Takigawa and Mogenson, 1977; Guyenet and Aghajanian, 1978; German et al., 1980; Maeda and Mogenson, 1980; Yim and Mogenson, 1980), unmyelinated ( Hattori et al., 1991) axons with relatively long refractory periods ( Anderson et al., 1996) that ascend from the midbrain to the forebrain ( Ungerstedt, 1971). The series-circuit hypothesis ( Shizgal et al., 1980; Wise, 1980; Bielajew and Shizgal, 1986) was proposed to reconcile the pharmacological data implicating dopaminergic neurons in MFB self-stimulation with the portrayal that has emerged from the psychophysical studies. The Series-Circuit Model of Intracranial Self-Stimulation

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Richardson, D. S., Guan, W., Matsumoto, K., Pan, C., Chung, K., Ertürk, A., et al. (2021). Tissue clearing. Nat. Rev. Methods Primers 1:84. doi: 10.1038/s43586-021-00080-9 Coenen, V., Hurwitz, T., Panksepp, J., Mädler, B., and Honey, C. (2009b). Medial forebrain bundle stimulation elicits psychotropic side effects in Subthalamic Nucleus Deep Brain Stimulation for PD – new insights through Diffusion Tensor Imaging. Akt Neurol. 36, s–0029–1238842. doi: 10.1055/s-0029-1238842 Yan, H.-C., Cao, X., Das, M., Zhu, X.-H., and Gao, T.-M. (2010). Behavioral animal models of depression. Neurosci. Bull. 26, 327–337. doi: 10.1007/s12264-010-0323-7

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The animal study that generated the publicly available dataset was reviewed and approved by the Animal Research Ethics Committee, Concordia University. Author Contributions Salience memories formed by value, novelty and aversiveness jointly shape object responses in the prefrontal cortex and basal ganglia The most widely used psychiatric diagnostic manual lists anhedonia as one the two cardinal depressive symptoms ( American Psychiatric Association, 2013). Originally coined as the complete loss of pleasure ( Ribot, 1897), the concept of anhedonia has broadened and differentiated ( Treadway et al., 2012; Zald and Treadway, 2017). In contemporary research anhedonia is now operationalized using multiple sub-constructs. Among them are consummatory anhedonia: a reduction in hedonic perception, or enjoyment of rewards (the original definition); motivational anhedonia: a reduced capacity to expend effort in reward pursuit; and decisional anhedonia: an impairment in reward learning and goal selection ( Zald and Treadway, 2017). Kim, K. M., Baratta, M. V., Yang, A., Lee, D., Boyden, E. S., and Fiorillo, C. D. (2012). Optogenetic mimicry of the transient activation of dopamine neurons by natural reward is sufficient for operant reinforcement. PLoS One 7:e33612. doi: 10.1371/journal.pone.0033612 Choice performance, following training (>5 sessions per set), showed robust preference for good over aversive (airpuff) or neutral objects as expected. In choices between neutral and airpuff objects there was also a significant preference for neutral object in both monkeys (Fig. 2d, e). This means that in both monkeys airpuff objects had a ‘lower’ valence compared to neutral objects (Fig. 2d, e). The choice bias was stronger in Monkey B compared to Monkey R (Monkey B %98, Monkey R %68). Nevertheless, and despite their lower valence, free viewing showed a significantly larger gaze bias toward airpuff compared to neutral objects in monkey B. In monkey R there was also a positive trend toward higher salience for airpuff vs neutral objects that did not reach significance. These results suggest airpuff objects to have an overall positive salience (higher gaze bias than neutral) despite their negative valence (lower value than neutral). Analysis of saccade reaction time for airpuff, neutral and good objects also showed faster saccades toward airpuff objects compared to neutral objects similar to saccade reaction time to good objects consistent with attentional salience observed in free viewing (Supplementary Fig. 4).

Feltz, P., and Albe-Fessard, D. (1972). A study of an ascending nigro-caudate pathway. Electroencephalogr. Clin. Neurophysiol. 33, 179–193. doi: 10.1016/0013-4694(72)90045-4 Breton, Y.-A., Conover, K., and Shizgal, P. (2014). The effect of probability discounting on reward seeking: a three-dimensional perspective. Front. Behav. Neurosci. 8:284. doi: 10.3389/fnbeh.2014.00284 Solomon, R. B., Conover, K., and Shizgal, P. (2017). Valuation of opportunity costs by rats working for rewarding electrical brain stimulation. PLoS One 12:e0182120. doi: 10.1371/journal.pone.0182120 Deutsch, J. A., Adams, D. W., and Metzner, R. J. (1964). Choice of intracranial stimulation as a function of delay between stimulations and strength of competing drive. J. Comparat. Physiol. Psychol. 57, 241–243. doi: 10.1037/h0047915 Fenoy, A. J., Schulz, P., Selvaraj, S., Burrows, C., Spiker, D., Cao, B., et al. (2016). Deep brain stimulation of the medial forebrain bundle: Distinctive responses in resistant depression. J. Affect. Disord. 203, 143–151. doi: 10.1016/j.jad.2016.05.064

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Huston, J. P. (1982). “Searching for the neural mechanism of reinforcement (of ‘stamping in’),” in The Neural Basis of Feeding and Reward, eds B. G. Hoebel and D. Novin (Florida, Fl: Academic Press), 75–83. In agreement with the Freiburg group and Panksepp, we hold that research on MFB self-stimulation in rodents will continue to have translational implications. We hope that future research into this seminal phenomenon, coupled with allied experimental work in non-human primates and humans, will yield a fuller understanding, both of the psychological and neural mechanisms underlying the antidepressant effect of deep-brain stimulation, and of the neural foundations of reward and motivation. Data Availability Statement Franklin, K. B. (1978). Catecholamines and self-stimulation: reward and performances effects dissociated. Pharmacol. Biochem. Behav. 9, 813–820. doi: 10.1016/0091-3057(78)90361-1The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Publisher’s Note Harmer, C. J., Duman, R. S., and Cowen, P. J. (2017). How do antidepressants work? New perspectives for refining future treatment approaches. Lancet Psychiat. 4, 409–418. doi: 10.1016/S2215-0366(17)30015-9

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Takigawa, M., and Mogenson, G. J. (1977). A study of inputs to antidromically identified neurons of the locus coeruleus. Brain Res. 135, 217–230. doi: 10.1016/0006-8993(77)91027-7Yim, C. Y., and Mogenson, G. J. (1980). Electrophysiological studies of neurons in the ventral tegmental area of Tsai. Brain Res. 181, 301–313. doi: 10.1016/0006-8993(80)90614-9 Huston, J. P., and Borbély, A. A. (1973). Operant conditioning in forebrain ablated rats by use of rewarding hypothalamic stimulation. Brain Res. 50, 467–472. doi: 10.1016/0006-8993(73)90753-1 Substantia nigra (SN) recording localization in both subjects were done using T1- and T2- weighted MRI (4.7 T, Bruker). T2- weighted MRI is especially useful for imaging SNr area due to higher iron content 60. During imaging, the recoding chambers wer Niyogi, R. K., Breton, Y. A., Solomon, R. B., Conover, K., Shizgal, P., and Dayan, P. (2013). Optimal indolence: a normative microscopic approach to work and leisure. J. R. Soc. Interface 11, 20130969–20130969. doi: 10.1016/S0166-4328(02)00282-6 Fouriezos, G., Bielajew, C., and Pagotto, W. (1990). Task difficulty increases thresholds of rewarding brain stimulation. Behav. Brain Res. 37, 1–7. doi: 10.1016/0166-4328(90)90066-n