A “Sample-and-Hold” Pulse-Counting Integrator as a Mechanism for Graded Memory Underlying Sensorimotor Adaptation

• Published in: Neuron (Cambridge, Mass.) Mass.), 2006-02, Vol.49 (4), p.577-588
• Main Authors: Oestreich, Jörg, Dembrow, Nikolai C., George, Andrew A., Zakon, Harold H.
• Format: Article
• Language: English
• Subjects: Acclimatization; Action Potentials - drug effects; Action Potentials - physiology; Action Potentials - radiation effects; Amino Acid Sequence; Animals; Behavior; Behavior, Animal; Biological Clocks - physiology; Calcium - metabolism; Calcium Channel Blockers - pharmacology; Dose-Response Relationship, Drug; Dose-Response Relationship, Radiation; Electric Fish; Electric Organ - drug effects; Electric Organ - physiology; Electric Organ - radiation effects; Excitatory Amino Acid Agonists - pharmacology; Excitatory Amino Acid Antagonists - pharmacology; Flufenamic Acid - pharmacology; In Vitro Techniques; Medulla Oblongata - cytology; Memory - physiology; Models, Neurological; N-Methylaspartate - pharmacology; Neurons - drug effects; Neurons - physiology; Neurons - radiation effects; omega-Conotoxin GVIA - pharmacology; Physical Stimulation - methods; Piperazines - pharmacology; Statistical analysis; SYSNEURO; TRPM Cation Channels - antagonists & inhibitors; TRPM Cation Channels - metabolism
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2006.01.027

The mechanisms behind the induction of cellular correlates of memory by sensory input and their contribution to meaningful behavioral changes are largely unknown. We previously reported a graded memory in the form of sensorimotor adaptation in the electromotor output of electric fish. Here we show that the mechanism for this adaptation is a synaptically induced long-lasting shift in intrinsic neuronal excitability. This mechanism rapidly integrates hundreds of spikes in a second, or gradually integrates the same number of spikes delivered over tens of minutes. Thus, this mechanism appears immune to frequency-dependent fluctuations in input and operates as a simple pulse counter over a wide range of time scales, enabling it to transduce graded sensory information into a graded memory and a corresponding change in the behavioral output. This adaptation is based on an NMDA receptor-mediated change in intrinsic excitability of the postsynaptic neurons involving the Ca 2+-dependent activation of TRP channels.