The organization of defensive behavior elicited by optogenetic excitation of rat lateral or ventrolateral periaqueductal gray.

Abstract

Rodents display characteristic defense responses to predators that are influenced by predatory imminence. The midbrain periaqueductal gray (PAG) serves an important role controlling these responses. The most influential model states that variations in defensive topography are due to distinct PAG regions: ventrolateral PAG (VLPAG) controls postencounter defense, such as freezing and immobility, whereas lateral PAG (LPAG) controls circa-strike defense, such as escape and flight. Here we used channel rhodopsin (ChR2) stimulation to probe the structure of defensive behavior controlled by LPAG and VLPAG. Suprathreshold LPAG stimulation evoked circa-strike defense that was replaced by freezing at stimulation offset. Suprathreshold VLPAG stimulation evoked postencounter--freezing and immobility--but never circa-strike defense. More interestingly, the topography of defensive behavior evoked from LPAG scaled with variations in 465 nm light power. As light power increased, LPAG animals expressed the full defensive syntax of freezing then activity then flight characteristic of increasing predatory imminence. In contrast, the frequency, not topography, of defensive behavior evoked from VLPAG scaled with variations in light power. These findings suggest that LPAG and VLPAG can control variations in defense with increasing predatory imminence in 2 ways. First, consistent with past models, topographical variation can be assembled from different defensive responses controlled by the LPAG (circa-strike) and VLPAG (postencounter). Second, topographical variation can be assembled from variations in LPAG activity itself. (PsycINFO Database Record

The periaqueductal gray and primal emotional processing critical to influence complex defensive responses, fear learning and reward seeking

“…On the other hand, the ventrolateral PAG has been shown to be involved in organizing immobility and freezing during the post-defense recuperative-like quiescent behavior (Assareh et al, 2016;Bandler and Keay, 1996;Bittencourt et al, 2004;Carrive, 1993). However, in contrast to this idea, recent observations by our lab have suggested that the ventrolateral PAG is also seemingly involved in organizing freezing during a predatory encounter (S. R. Mota-Ortiz and N.S.…”

“…In other words, "postencounter" reflects the initial detection of the potential threat, whereas "circa-strike" is associated with the direct interaction with the predator (i.e., when the predator attacks). Accordingly, both post-encounter and circa-strike defensive behaviors have been ascribed to the dorsomedial, dorsolateral and lateral columns of the PAG, where electrical, pharmacological and optogenetic stimulation have been shown to produce freezing, escape and flight behavior in the absence of a predatory threat (Assareh et al, 2016;Bandler and Keay, 1996;Bittencourt et al, 2004;Carrive, 1993;Deng et al, 2016). Interestingly, dorsal and lateral PAG stimulation may evoke either freezing or escape and jumps, where low magnitude stimuli produced freezing, and slightly higher intensities evoked circa-strike responses (Assareh et al, 2016;Bittencourt et al, 2004;Vianna et al, 2001).…”

“…Accordingly, both post-encounter and circa-strike defensive behaviors have been ascribed to the dorsomedial, dorsolateral and lateral columns of the PAG, where electrical, pharmacological and optogenetic stimulation have been shown to produce freezing, escape and flight behavior in the absence of a predatory threat (Assareh et al, 2016;Bandler and Keay, 1996;Bittencourt et al, 2004;Carrive, 1993;Deng et al, 2016). Interestingly, dorsal and lateral PAG stimulation may evoke either freezing or escape and jumps, where low magnitude stimuli produced freezing, and slightly higher intensities evoked circa-strike responses (Assareh et al, 2016;Bittencourt et al, 2004;Vianna et al, 2001). Recent findings in mice using optogenetic tools have shown that higher frequency or higher intensity optogenetic stimulation in the dorsal PAG induced running followed by post-stimulation freezing, with progressively increasing levels of freezing with increases in laser stimulation strength (Deng et al, 2016).…”

Genotype-dependent responsivity to inflammatory pain: A role for TRPV1 in the periaqueductal grey

“…used channel rhodopsin (ChR2) stimulation to probe defensive behaviour controlled by the LPAG; suprathreshold LPAG stimulation evoked escape-flight defence that was replaced by freezing at stimulation offset, hence providing more evidence that the LPAG is involved in mediating defence responses (Assareh et al, 2016).…”

Defensive Vocalizations and Motor Asymmetry Triggered by Disinhibition of the Periaqueductal Gray in Non-human Primates

“…For example, optogenetic activation of the lateral PAG in the rat induces both freezing, and flight behaviors, with higher irradiance needed to evoke flight as compared to freezing behavior (Assareh et al, 2016). Interestingly, these thresholds were lower in the lateral PAG as compared to the ventrolateral PAG.…”