Abstract
The periaqueductal gray (PAG) has a well-established role in pain processing, autonomic function and behavioral responses to fear. Anatomical work suggests the PAG may mediate food intake and reward processing as it has extensive reciprocal connections within brain circuits that mediate appetitive processes and consummatory behaviors such as prefrontal cortex, hypothalamus, amygdala, parabrachial nucleus (PBN) and ventral tegmental area (Kelley et al., 2005). Therefore, we investigated if the PAG of hungry rats has a functional role in appetitive and consummatory behaviors. To address this, PAG was pharmacologically inactivated during a spatial working memory task with muscimol (0.1–0.3 μg), a GABAA agonist via intracranial infusion. Inactivation of PAG led to reduced intake of food rewards and increased errors on this task. To focus on the specific effects PAG inactivation had on food consumption, PAG was inactivated during two separate food intake tasks in a separate group of rats. Again, PAG inactivation resulted in a significant decrease in food consumption, as well as an increased latency to consume food. We next investigated PAG neural responses to reward encounters. A different group of rats performed the same task used in Experiment 1 while the in vivo activity of PAG neurons was recorded. In a subset of PAG neurons, reward encounters elicited phasic excitation. A separate subset of PAG neurons were inhibited during reward encounters. These responses scaled with the size of the reward, with sustained excitation or inhibition in response to large rewards compared to small. Our data also show that separate groups of PAG neurons in awake behaving animals display either increased and decreased neural responses to reward encounters. Additionally, a proportion of neurons were modulated by the animals’ velocity. This study is the first to show that PAG neurons process reward-related information, perhaps to mediate consummatory behaviors related to food consumption.
Highlights
The periaqueductal gray (PAG) is a structure that has been long-known to play an important role in endogenous analgesia, vocalizations, defensive behaviors and autonomic regulation (Bandler and Depaulis, 1991; Behbehani, 1995)
It is connected to regions important for decision making, Periaqueductal Gray Involved in Feeding Behavior reward processing and motivation and basic homeostatic drives (e.g., the lateral hypothalamus and parabrachial nucleus (PBN), Behbehani et al, 1988; Krout et al, 1998)
While a vast literature supports the view that PAG mediates the processing of fear and pain information (Depaulis and Bandler, 2012), the present study provides the first clear evidence that PAG is important for processing appetitive information, such as palatable rewards
Summary
The periaqueductal gray (PAG) is a structure that has been long-known to play an important role in endogenous analgesia, vocalizations, defensive behaviors and autonomic regulation (Bandler and Depaulis, 1991; Behbehani, 1995). It is connected to regions important for decision making (e.g., medial prefrontal cortex and amygdala, Beitz, 1982; Rizvi et al, 1991; Rozeske et al, 2018), Periaqueductal Gray Involved in Feeding Behavior reward processing and motivation (e.g., the ventral tegmental area, VTA, Omelchenko and Sesack, 2010; Ntamati et al, 2018) and basic homeostatic drives (e.g., the lateral hypothalamus and parabrachial nucleus (PBN), Behbehani et al, 1988; Krout et al, 1998) These and other studies suggest that the PAG may play a functional role in mediating appetitive behaviors but there has not been much investigation of this hypothesis. It has been documented that expectancy of a food reward can activate endogenous opioid-mediated analgesia which is thought to be mediated by the PAG (Dum and Herz, 1984; Fields, 2004) and it is hypothesized that reward expectation elicits an analgesic response to allow an animal to ignore noxious stimuli and attend to a rewarding stimulus (Fields, 2007; Leknes and Tracey, 2008)
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