First evidence of neuronal connections between specific parts of the periaqueductal gray (PAG) and the rest of the brain in sheep: placing the sheep PAG in the circuit of emotion

Abstract

The periaqueductal gray (PAG) is a mesencephalic brain structure organised in subdivisions with specific anatomical connections with the rest of the brain. These connections support the different PAG functions and especially its role in emotion. Mainly described in territorial and predatory mammals, examination of the PAG connections suggests an opposite role of the ventral and the dorsal/lateral PAG in passive and active coping style, respectively. In mammals, the organisation of PAG connections may reflect the coping style of each species. Based on this hypothesis, we investigated the anatomical connections of the PAG in sheep, a gregarious and prey species. Since emotional responses expressed by sheep are typical of active coping style, we focused our interest on the dorsal and lateral parts of the PAG. After injection of fluorogold and fluororuby, the most numerous connections occurred with the anterior cingulate gyrus, the anterior hypothalamic region, the ventromedial hypothalamic nucleus and the PAG itself. Our observations show that the sheep PAG belongs to the neuronal circuit of emotion and has specific parts as in other mammals. However, unlike other mammals, we observed very few connections between PAG and either the thalamic or the amygdalar nuclei. Interestingly, when comparing across species, the PAG connections of sheep were noticeably more like those previously described in other social species, rabbits and squirrel monkeys, than those in territorial species, rats or cats.

Mutual interactions between cognition and welfare: The horse as an animal model

“…According to "affective neuroscience", the basic emotional circuits of mammalian brains show consistency along the evolutionary scale and studying the basic emotional systems of animals may help scientifically understand the foundations of the human mind (Panksepp, 2011b). The neuronal basis of the emotions has been explored and brain structures have been identified as being involved in the perception of stimuli (i.e., sensory cortex, Soudry et al, 2011;Grosso et al, 2015;Concina et al, 2019), processing and storage of the information (e.g., orbitofrontal cortex, amygdala and hippocampus; LeDoux, 2000;Barbas et al, 2011;Chaaya et al, 2018;Rolls, 2019), and expression of emotions (e.g., paraventricular nucleus of the hypothalamus that triggers endocrine responses, periaqueductal gray that triggers behavioural responses and medulla that triggers autonomic responses, Hagemann et al, 2003;Goldstein, 2010;Menant et al, 2016Menant et al, , 2018. Panksepp (2005Panksepp ( , 2011a has mapped several basic emotional circuits in mammals consisting of neuronal pathways that interconnect midbrain circuits concentrated in midbrain regions, such as periaqueductal gray, with various basal ganglia, such as amygdala, via the hypothalamus and thalamus.…”

Periaqueductal gray and emotions: the complexity of the problem and the light at the end of the tunnel, the magnetic resonance imaging

“…Thus, comparison of species is of particular importance to better describe and understand the brain and its role in the cognitive functions, as it has been reviewed in more and more papers [parental brain (Bales 2017); friendship (Brent et al 2014)]. This requires thorough knowledge of the behavior of different species using ethological approaches and to explore anatomical (Menant et al 2018) and functional (Najafi et al 2017) connections of different brain structures with the help of MRI and to develop postprocessing tools to get a more comprehensive picture of the various species.…”

“…The additional knowledge obtained with this method was that despite the similarities in the columnar structure of the PAG there appears to be different patterns of cortical connectivity between humans and non-human animals. We recently described specific connections between the PAG areas and the rest of the brains in sheep that was different from other mammals (Menant et al 2018). These differences could lead to alteration in the coping style, specific for each species (prey, predator, territorial, gregarious etc.…”

“…Thus, the dPAG could regulate fear during innate negative events and not during memory recall. The different subdivisions of the PAG participate in different neuronal circuits supported by their specific anatomical connections with the rest of the brain (Menant 2016a), which can differ between species (Menant et al 2018). Altogether, activation of the dPAG induces active responses, whereas the vPAG is responsible for immobility ( Figure 4).…”

Decreased Resting-State Functional Connectivity of Periaqueductal Gray in Temporal Lobe Epilepsy Comorbid With Migraine

“…The FG-traced neuron number within vlPAG will be used to identify the neural transmission activity of vlPAG-PPN pathway. This FG retrograde tracing method has been widely used to study the activity of neuronal connections between different parts within the brain associated with distinct functions (45)(46)(47). For comparison of the neural transmission activity of vlPAG-PPN pathway between normal rats and chronic epileptic rats, seizure stimulation activating vlPAG-PPN pathway should be similar in severity and duration.…”