Psychophysical inference of frequency-following fidelity in the neural substrate for brain stimulation reward

Solomon, Rebecca Brana; Trujillo-Pisanty, Ivan; Conover, Kent; Shizgal, Peter

doi:10.1016/j.bbr.2015.06.008

Cited by 13 publications

(38 citation statements)

References 66 publications

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“…The shape of the reward-mountain surface fitted to the oICSS data (Figs 5, S17-S22) resembles that of the surfaces fit to eICSS data reported previously [8, 37–39, 45, 46, 56, 57]. Time allocation falls as pulse-frequency is decreased and/or price is increased.…”

Section: Discussionsupporting

confidence: 75%

“…This firing frequency is the location parameter of the underlying reward-growth function. Given the exceptional frequency-following fidelity of the directly activated neurons subserving eICSS of the MFB [8], it is not unreasonable to assume that each pulse elicits an action potential in most or all of the directly stimulated MFB neurons when the pulse frequency equals . In contrast, the findings reviewed in section Parameters of the frequency-following function for oICSS of the supporting-information file argue that such an assumption is untenable in the case of oICSS of channelrhodopsin-2 expressing midbrain dopamine neurons.…”

Section: Resultsmentioning

confidence: 99%

“…Consequently, they have very high thresholds to excitation by extracellular currents. Robust ICSS of sites along the medial forebrain bundle (MFB) is observed using stimulation parameters too weak to produce substantial recruitment of dopaminergic fibers [8]. Moreover, estimates of recovery of refractoriness, conduction velocity, and frequency-following fidelity in the directly activated fibers underlying the rewarding effect implicate fibers that are myelinated and far more excitable than those of dopamine neurons [9–14].…”

Section: Introductionmentioning

confidence: 99%

“…The firing frequency of the activated neurons eventually rolls off as pulse frequency is increased sufficiently [8].…”

Section: Introductionmentioning

confidence: 99%

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The effect of dopamine transporter blockade on optical self-stimulation: behavioral and computational evidence for parallel processing in brain reward circuitry

Trujillo-Pisanty

Conover

Solis

et al. 2019

Preprint

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The neurobiological study of reward was launched by the discovery of intracranial self-stimulation (ICSS). Subsequent investigation of this phenomenon provided the initial link between reward-seeking behavior and dopaminergic neurotransmission. We re-evaluated this relationship by psychophysical, pharmacological, optogenetic, and computational means. In rats working for direct, optical activation of midbrain dopamine neurons, we varied the strength and opportunity cost of the stimulation and measured time allocation, the proportion of trial time devoted to reward pursuit. We found that the dependence of time allocation on the strength and cost of stimulation was similar formally to that observed when electrical stimulation of the medial forebrain bundle served as the reward. When the stimulation is strong and cheap, the rats devote almost all their time to reward pursuit; time allocation falls off as stimulation strength is decreased and/or its opportunity cost is increased. A 3D plot of time allocation versus stimulation strength and cost produces a surface resembling the corner of a plateau (the “reward mountain”). We show that dopamine-transporter blockade shifts the mountain along both the strength and cost axes in rats working for optical activation of midbrain dopamine neurons. In contrast, the same drug shifted the mountain uniquely along the opportunity-cost axis when rats worked for electrical MFB stimulation in a prior study. Dopamine neurons are an obligatory stage in the dominant model of ICSS, which positions them at a key nexus in the final common path for reward seeking. This model fails to provide a cogent account for the differential effect of dopamine transporter blockade on the reward mountain. Instead, we propose that midbrain dopamine neurons and neurons with non-dopaminergic, MFB axons constitute parallel limbs of brain-reward circuitry that ultimately converge on the final-common path for the evaluation and pursuit of rewards. Author summary To succeed in the struggle for survival and reproductive success, animals must make wise choices about which goals to pursue and how much to pay to attain them. How does the brain make such decisions and adjust behaviour accordingly? An animal model that has long served to address this question entails delivery of rewarding brain stimulation. When the probe is positioned appropriately in the brain, rats will work indefatigably to trigger such stimulation. Dopamine neurons play a crucial role in this phenomenon. The dominant model of the brain circuitry responsible for the reward-seeking behavior treats these cells as a gateway through which the reward-generating brain signals must pass. Here, we challenge this idea on the basis of an experiment in which the dopamine neurons were activated selectively and directly. Mathematical modeling of the results argues for a new view of the structure of brain reward circuitry. On this view, the pathway(s) in which the dopamine neurons are embedded is one of a set of parallel channels that process reward s...

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Section: Discussionsupporting

confidence: 75%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“…The firing frequency of the activated neurons eventually rolls off as pulse frequency is increased sufficiently [8].…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

The effect of dopamine transporter blockade on optical self-stimulation: behavioral and computational evidence for parallel processing in brain reward circuitry

Trujillo-Pisanty

Conover

Solis

et al. 2019

Preprint

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show abstract

“…Previous analysis of these data has primarily focused on behaviour during test trials, and in particular on responses occurring after the initial responses (Niyogi et al, 2014a;Niyogi et al, 2014b;Solomon et al, 2015;Solomon et al, 2017). Following Breton, 2013, we instead considered all trial types, and primarily focused on initial responses, since they reflect the subjects' beliefs about the likely worth of a trial before they encounter any within-trial information.…”

Section: Subjects Learn the Task Transition Structurementioning

confidence: 99%

Forgetful inference in a sophisticated world model

Ahilan

Solomon

Breton

et al. 2018

Preprint

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Humans and other animals are able to discover underlying statistical structure in their environments and exploit it to achieve efficient and effective performance. However, such structure is often difficult to learn and use because it is obscure, involving long-range temporal dependencies. Here, we analysed behavioural data from an extended experiment with rats, showing that the subjects learned the underlying statistical structure, albeit suffering at times from immediate inferential imperfections as to their current state within it. We accounted for their behaviour using a Hidden Markov Model, in which recent observations are integrated with the recollections of an imperfect memory. We found that over the course of training, subjects came to track their progress through the task more accurately, a change that our model largely attributed to decreased forgetting. This 'learning to remember' decreased reliance on recent observations, which may be misleading, in favour of a longer-term memory. Author summaryHumans and other animals possess the remarkable ability to find and exploit patterns and structures in their experience of a complex and varied world. However, such structures are often temporally extended and latent or hidden, being only partially correlated with immediate observations of the world. This makes it essential to integrate current and historical information, and creates a challenging statistical and computational problem.Here, we examine the behaviour of rats facing a version of this challenge posed by a brain-stimulation reward task. We find that subjects learned the general structure of the task, but struggled when immediate observations were misleading. We captured this behaviour with a model in which subjects integrated evidence from their observations together with a memory whose imperfections accounted for their errors.The subjects' performance improved markedly over successive sessions, allowing them to overcome misleading observations. According to the model, this arose from a process of 'learning to remember' in which subjects became better at employing more reliable past observations to determine the hidden state of the world.

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The neural substrates for the rewarding and dopamine-releasing effects of medial forebrain bundle stimulation have partially discrepant frequency responses

Cossette

Conover

Shizgal

2016

Behavioural Brain Research

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Psychophysical inference of frequency-following fidelity in the neural substrate for brain stimulation reward

Cited by 13 publications

References 66 publications

The effect of dopamine transporter blockade on optical self-stimulation: behavioral and computational evidence for parallel processing in brain reward circuitry

The effect of dopamine transporter blockade on optical self-stimulation: behavioral and computational evidence for parallel processing in brain reward circuitry

Forgetful inference in a sophisticated world model

The neural substrates for the rewarding and dopamine-releasing effects of medial forebrain bundle stimulation have partially discrepant frequency responses

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