Detection of an inhibitory cortical gradient underlying peak shift in learning: A neural basis for a false memory

• Published in: Neurobiology of learning and memory 2012-11, Vol.98 (4), p.368-379
• Main Authors: Miasnikov, Alexandre A., Weinberger, Norman M.
• Format: Article
• Language: English
• Subjects: Acetylcholine; Acoustic Stimulation; Animal models; Animals; Association Learning - physiology; Associative learning; Auditory cortex; Auditory Cortex - physiology; Auditory discrimination learning; Basal Nucleus of Meynert - physiology; Behavioral psychophysiology; Biological and medical sciences; Cholinergic Neurons - physiology; Conditioning; Conditioning, Classical - physiology; Cortex (auditory); Discrimination Learning - physiology; Electric Stimulation; Evoked potentials; Evoked Potentials, Auditory - physiology; Frequency generalization; Fundamental and applied biological sciences. Psychology; Generalization, Stimulus - physiology; Implanted memory; Learning; Male; Memory; Mental Recall - physiology; Nervous system; Neurobiology; Nucleus basalis; Psychology. Psychoanalysis. Psychiatry; Psychology. Psychophysiology; Rats; Rats, Sprague-Dawley; Reinforcement; Repression, Psychology; Respiration; Sensory perception
• ISSN: 1074-7427; 1095-9564
• DOI: 10.1016/j.nlm.2012.10.001

► Peak shift in stimulus generalization is an experiential error, i.e., false memory. ► We produced peak shift by giving many different tones before training with 1tone. ► Repeated tones induced an inhibitory neural gradient in primary auditory cortex. ► This specific inhibitory neural gradient accounted for the behavioral peak shift. ► An animal model to discover the neural bases of selected false memories is at hand. Experience often does not produce veridical memory. Understanding false attribution of events constitutes an important problem in memory research. “Peak shift” is a well-characterized, controllable phenomenon in which human and animal subjects that receive reinforcement associated with one sensory stimulus later respond maximally to another stimulus in post-training stimulus generalization tests. Peak shift ordinarily develops in discrimination learning (reinforced CS+, unreinforced CS−) and has long been attributed to the interaction of an excitatory gradient centered on the CS+ and an inhibitory gradient centered on the CS−; the shift is away from the CS−. In contrast, we have obtained peak shifts during single tone frequency training, using stimulation of the cholinergic nucleus basalis (NB) to implant behavioral memory into the rat. As we also recorded cortical activity, we took the opportunity to investigate the possible existence of a neural frequency gradient that could account for behavioral peak shift. Behavioral frequency generalization gradients (FGGs, interruption of ongoing respiration) were determined twice before training while evoked potentials were recorded from the primary auditory cortex (A1), to obtain a baseline gradient of “habituatory” neural decrement. A post-training behavioral FGG obtained 24h after three daily sessions of a single tone paired with NB stimulation (200trials/day) revealed a peak shift. The peak of the FGG was at a frequency lower than the CS while the cortical inhibitory gradient was at a frequency higher than the CS frequency. Further analysis indicated that the frequency location and magnitude of the gradient could account for the behavioral peak shift. These results provide a neural basis for a systematic case of memory misattribution and may provide an animal model for the study of the neural bases of a type of “false memory”.