Why, where and how do top-down and bottom-up signals interact in the primate brain?

Here we propose a roadmap for addressing hierarchical predictive coding theory (hPC) in the primate brain, theorizing that perception arises from the integration of bottom-up (BU) pathways carrying sensory evidence with top-down (TD) pathways carrying priors and expectations. However, given the conceptual importance of hPC for higher cognitive function in humans there is surprising little evidence concerning the location and functional mechanisms underlying such BU-TD integration. This will be overcome by parallel experiments in humans and non-human primates (NHPs). Molecular characterization in NHP of cortico-cortical BU and TD projection cell types will allow tracing these circuits and exerting causal control to explore functional mechanisms in visual paradigms in behaving NHPs. Identical paradigms in human subjects undergoing ultra-high field laminar fMRI scanning will indicate homologous pathways in the human brain. In NHP and human, long-distance priors and expectations suggest that the claustrum is involved in hPC. Recent connectomic and transcriptomic characterisation of cortical claustral cortical loops will enable a similar approach to explore these pathways’ participation in the integration of TD and BU signals as used in the cortico-cortical pathways. Progress in primate hPC will further emphasise the synergy between neurobiology and artificial intelligence with important consequences for both domains.