Common Fronto-temporal Effective Connectivity in Humans and Monkeys

Abstract

Highlights 22 • Privileged human auditory to inferior frontal connectivity, linked to monkeys 23 • Common auditory to parahippocampal effective connectivity in both species 24 • Greater lateralization in human effective connectivity, more symmetrical in monkeys 25 • Human fronto-temporal network function rooted in evolutionarily conserved signature 26 27 eTOC short summary 28 Functional connectivity between regions crucial for language and declarative memory is thought to 29 have substantially differentiated in humans. Using a new technique to similarly visualize directional 30 effective connectivity in humans and monkeys, we found remarkably comparable connectivity patterns 31 in both species between fronto-temporal regions crucial for cognition. 32 33 ABSTRACT 36 Cognitive pathways supporting human language and declarative memory are thought to have uniquely 37 evolutionarily differentiated in our species. However, cross-species comparisons are missing on site-38 specific effective connectivity between regions important for cognition. We harnessed a new approach 39 using functional imaging to visualize the impact of direct electrical brain stimulation in human 40 neurosurgery patients. Applying the same approach with macaque monkeys, we found remarkably 41 comparable patterns of effective connectivity between auditory cortex and ventro-lateral prefrontal 42 cortex (vlPFC) and parahippocampal cortex in both species. Moreover, in humans electrical 43 tractography revealed rapid evoked potentials in vlPFC from stimulating auditory cortex and speech 44 sounds drove vlPFC, consistent with prior evidence in monkeys of direct projections from auditory 45 cortex to vocalization responsive regions in vlPFC. The results identify a common effective 46 connectivity signature that from auditory cortex is equally direct to vlPFC and indirect to the homology, convergence or divergence, can be of substantial theoretical significance: Within the motor 52 domain, human and nonhuman primates have direct cortico-spinal projections subserving fine 53 movement control that are indirect in rodents 1 . Also, human laryngeal motor cortex projects directly to 54 a brain stem nucleus (ambiguus) controlling laryngeal muscles 2 . Such projections for vocal production 55 are more indirect in nonhuman primates 3 and rodents 4 , shedding light on human speech evolution 5 . 56 Language defines us as a species and because of its prominent role in declarative memory 57 substantial evolutionary differentiation of human cognitive pathways is expected. Comparative studies 58 often see considerable levels of evolutionary conservation alongside insights on species-specific 59 differences 6-12 . Yet, certain cross-species comparisons are missing, such as on the impact of directed 60 effective connectivity with the required precision of site-specific perturbation that can be applied to 61 both human and nonhuman primates. Thereby, the question on the extent of differentiation versus 62 conservation in primate fronto-temporal systems-although crucial fo...

Categorizing human vocal signals depends on an integrated auditory‐frontal cortical network

“…Beside the distributed activity pattern in bilateral AC and IFC, we finally determined the functional connectivity between these regions of the voice‐processing network. The AC and IFC are anatomically and functionally connected during auditory processing as shown in nonhuman primates (Medalla & Barbas, 2014; Plakke & Romanski, 2014), and a similar network is suggested for humans (Rocchi et al, 2020). We here, for the first time, characterize the direction of functional modulation of auditory‐frontal connections during task‐based vocal‐sound processing and systematically modulated the relevance of vocal sounds for the ongoing task.…”

A data resource from concurrent intracranial stimulation and functional MRI of the human brain

“…This results in the relative oversampling of the few locations that are typically targeted in the respective disorders (in our case, medial temporal lobe and medial frontal cortex); on the other hand, it has the benefit of accruing data across subjects who have stimulation in anatomically overlapping regions. Third, depending on the details of the electrode design and the stimulation parameters, electrical stimulation can result in substantial current spread (at least ~3 mm 52 ), and in any case it is not selective for particular cell types and includes stimulated fibers of passage, unlike optogenetics. Fourth, the implanted electrodes typically introduce susceptibility-derived artifacts (including geometrical distortion and signal loss) on the BOLD-fMRI scan, as we noted earlier.…”

Combining Brain Perturbation and Neuroimaging in Non-human Primates

“…For instance, the stimulation strength thresholds at which measurable brain activations are evoked may be significantly higher in anesthetized animals compared to awake ones (Murris et al, 2020;Premereur et al, 2015). Moreover, both the pattern and amplitude of perturbation-induced activity changes can vary as a function of brain state (Moeller et al, 2009;Murris et al, 2020;Petkov et al, 2015;Premereur et al, 2015;Rocchi et al, 2021).…”

“…Recently, es-fMRI has been directly compared between monkeys and humans. Rocchi et al (2021) assessed fMRI results from stimulation of monkey and human auditory cortex (Figure 5). They assessed the pattern of es-fMRI effects in frontal and medial temporal lobe regions evoked by stimulating different sites in the auditory cortex on the supratemporal plane.…”

“…In electrophysiological studies, the distinction between antidromic and orthodromic stimulation effects is sometimes made based on the shape and selectivity of the stimulation-evoked response, or the interaction with ongoing sensory processes (Klink et al, 2017). The rather low temporal resolution of fMRI makes it difficult to derive similar distinctions directly from the imaging signal, but a comparison of es-fMRI and electrophysiological signatures may allow inferences about the nature of es-fMRI effects (Rocchi et al, 2021).…”