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The cognitive basis of intracranial self-stimulation of midbrain dopamine neurons

Samuel J. MillardiD, Ivy B. Hoang, Zara Greer, Shayna L. O’ConnoriD, Kate M. WassumiD, Morgan H. JamesiD, David J. BarkeriD, Melissa J. SharpeiD

Abstract

Recently there has been a reckoning in the dopamine field. This has suggested that the dopamine prediction error may function as a teaching signal, without endowing preceding events with value. We studied the cognitive basis of intracranial self-stimulation (ICSS), a setting where dopamine appears to be valuable. Physiological frequencies seen during reinforcement learning did not support robust ICSS or promote behavior that would indicate the stimulation was represented as a meaningful reward in a specific or general sense. This was despite demonstrating that this same physiologically-relevant signal could function as a teaching signal. However, supraphysiological frequencies supported robust ICSS where the stimulation was represented as a specific sensory event, which acted as a goal to motivate behavior. This demonstrates that dopamine neurons only support ICSS at supraphysiological frequencies, and in a manner that does not reflect our subjective experience with endogenous firing of dopamine neurons during reinforcement learning. One sentence summaryDopamine neurons only support ICSS at supraphysiological frequencies and in a manner not reflecting dopamines role in learning.

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