Behavioral and autonomic dynamics during contextual fear conditioning in mice.

Aversive conditioning to contextual stimulation was performed in mice implanted with ECG transmitters to investigate heart rate (HR) and behavioral responses during contextual retention. The dynamics of HR were analyzed by advanced nonlinear techniques to uncover central neuroautonomic outflow inferred from its sympathetic (SNS) and parasympathetic (PNS) projection onto the sinus node of the heart. Mice experienced a single foot shock (US, unconditioned stimulus) either immediately (USi) or late (USl) after placement in the conditioning context. Contextual memory was tested 24 h after training by reexposure to the conditioning context for 32 min. Only mice that experienced the USl exhibited a pronounced and sustained behavioral suppression (immobility) indicative of conditioned contextual fear. In contrast, HR was initially close to its maximal physiological limit (approximately 800 bpm) in all groups, and recovery towards baseline levels was sluggish, the most pronounced delay observed in the USl group. The results demonstrate that behavioral immobility was associated with maximum activation of autonomic system output in response to contextual reexposure. However, advanced complexity analysis of the variability of HR revealed uniform or stereotyped dynamical properties that were interpreted to reflect a generalized state of anticipatory emotional arousal experienced during reexposure to contextual stimuli. It is concluded that the dynamics of HR is a highly sensitive index of the autonomic nervous system response and emotional state elicited by sensory stimulation of an unfamiliar environment.