We live in a microbial world with trillions of microbes in and around us helping to digest food and regulating the immune system. Emerging data also suggest the critical influence of the gut microbiota on the brain impacting on behaviour and mental health. For example, the absence of gut microbes in experimentally derived germ-free mice results in impaired behaviours including reduced or complete lack of social interactions. Conversely, supplementation of deficient gut microbiota with probiotics and/or specific bacterial strains can restore social function. Despite a surge in such correlative demonstrations, the underlying neuronal mechanisms remain to be defined. We hypothesise, that one key central nervous system pathway for gut microbial influence on social behaviour originates from the vagus nerve through to the brainstem solitary nucleus (NTS) and its socially-relevant afferent region the paraventricular hypothalamus (PVN). We aim to identify cell-type selective synaptic connections of this social gut microbial-brain pathway. We combined gut microbiota manipulation with behavioural testing, neuronal activity tagging, viral labelling and multichannel immunohistochemistry to explore the impact of antibiotics-mediated gut microbiota depletion on social behaviour and neuronal activity in adult mice of both sexes. First, we demonstrate that antibiotics altered the pattern of social interactions. Second, we observed differential neuronal cFos-activation in the NTS and PVN in antibiotics-treated vs control mice. Third, we uncovered molecularly diverse NTS neuron types projecting to the PVN. Our findings indicate alterations of social behaviour and related neuronal activity by gut microbial status, likely supported by diverse neuronal populations along the gut-vagus-NTS-PVN pathway.