PT  - JOURNAL ARTICLE
AU  - Thomas C. Watson
AU  - Nadia L Cerminara
AU  - Bridget M. Lumb
AU  - Richard Apps
TI  - Neural correlates of fear in the periaqueductal gray.
AID  - 10.1523/JNEUROSCI.1100-16.2016
DP  - 2016 Nov 09
TA  - The Journal of Neuroscience
PG  - 1100-16
4099  - http://www.jneurosci.org/content/early/2016/11/09/JNEUROSCI.1100-16.2016.short
4100  - http://www.jneurosci.org/content/early/2016/11/09/JNEUROSCI.1100-16.2016.full
AB  - The dorsal and ventral periaqueductal gray (PAG) are embedded in distinct survival networks that co-ordinate, respectively, innate and conditioned fear-evoked freezing. However, the information encoded by the PAG during these survival behaviors is poorly understood. Recordings in the dorsal and ventral PAG in rats revealed differences in neuronal activity associated with the two behaviors. During innate fear, neuronal responses were significantly greater in the dorsal as compared to the ventral PAG. Following associative fear conditioning, and during early extinction, when freezing was maximal, a field potential was evoked in the PAG by the auditory fear conditioned stimulus (CS). With repeated presentations of the unreinforced CS animals displayed progressively less freezing accompanied by a reduction in event-related field potential amplitude. During early extinction the majority of dorsal and ventral PAG units increased their firing frequency but spike-triggered averaging showed that only ventral activity during the presentation of the CS was significantly coupled to EMG-related freezing behavior. This PAG-EMG coupling was only present for the onset of freezing activity during the CS in early extinction. During late extinction, a sub-population of units in the ventral and dorsal PAG continued to show CS-evoked responses i.e. were extinction resistant. Overall, these findings support roles for the dorsal PAG in innate and conditioned fear and for the ventral PAG in initiating but not maintaining the drive to muscles to generate conditioned freezing. The existence of extinction-susceptible and extinction-resistant cells also suggests the PAG plays a role in encoding fear memories.SIGNIFICANCE STATEMENTThe periaqueductal gray (PAG) orchestrates survival behaviors; with dorsal and ventral PAG concerned respectively with innate and learnt fear responses. We recorded neural activity from dorsal and ventral PAG in rats during the expression of innate fear and extinction of learnt freezing. Cells in dorsal PAG responded more robustly during innate fear but dorsal and ventral PAG both encoded the time of the conditioned stimulus during early extinction and displayed extinction sensitive and resistant characteristics. Only ventral PAG discharge was correlated to muscle activity but this was limited to the onset of conditioned freezing. The data suggest the roles of dorsal and ventral PAG in fear behavior are more complex than previously thought, including a potential role in fear memory.