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. 2021 Mar 3;109(5):852-868.e8.
doi: 10.1016/j.neuron.2020.12.026. Epub 2021 Jan 21.

Common fronto-temporal effective connectivity in humans and monkeys

Francesca Rocchi  1 , Hiroyuki Oya  2 , Fabien Balezeau  3 , Alexander J Billig  4 , Zsuzsanna Kocsis  5 , Rick L Jenison  6 , Kirill V Nourski  7 , Christopher K Kovach  8 , Mitchell Steinschneider  9 , Yukiko Kikuchi  3 , Ariane E Rhone  8 , Brian J Dlouhy  7 , Hiroto Kawasaki  8 , Ralph Adolphs  10 , Jeremy D W Greenlee  7 , Timothy D Griffiths  11 , Matthew A Howard 3rd  12 , Christopher I Petkov  13
Affiliations

Common fronto-temporal effective connectivity in humans and monkeys

Francesca Rocchi et al. Neuron. .

Abstract

Human brain pathways supporting language and declarative memory are thought to have differentiated substantially during evolution. However, cross-species comparisons are missing on site-specific effective connectivity between regions important for cognition. We harnessed functional imaging to visualize the effects of direct electrical brain stimulation in macaque monkeys and human neurosurgery patients. We discovered comparable effective connectivity between caudal auditory cortex and both ventro-lateral prefrontal cortex (VLPFC, including area 44) and parahippocampal cortex in both species. Human-specific differences were clearest in the form of stronger hemispheric lateralization effects. In humans, electrical tractography revealed remarkably rapid evoked potentials in VLPFC following auditory cortex stimulation and speech sounds drove VLPFC, consistent with prior evidence in monkeys of direct auditory cortex projections to homologous vocalization-responsive regions. The results identify a common effective connectivity signature in human and nonhuman primates, which from auditory cortex appears equally direct to VLPFC and indirect to the hippocampus. VIDEO ABSTRACT.

Keywords: cognition; declarative memory; evolution; frontal cortex; hippocampus; language; neural principles; neuroimaging; neurophysiology.

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Conflict of interest statement

Declaration of interests The authors declare no competing interests.

Figures

None
Graphical abstract
Figure 1
Figure 1
Illustrated hypotheses involving effective connectivity from auditory cortex to VLPFC and MTL areas in humans and monkeys (A) Hypothesis 1 predicts stronger effective connectivity from stimulating auditory cortex on human VLPFC areas 44/45 than in monkeys, because of the prominence of the dorsal pathway in humans interconnecting these areas with auditory cortex. By comparison, the ventral pathway interconnecting auditory cortex with areas such as the frontal operculum (FOP) is structurally dominant in nonhuman primates. Thus, by this hypothesis, effective connectivity in the monkeys could be stronger in FOP than areas 44/45. MTL effects by some accounts are expected to be stronger in human hippocampal subregions than adjacent areas, such as the parahippocampal gyrus (PHG). In monkeys, the reverse pattern is expected; see text. (B) Hypothesis 2 predicts cross-species correspondences in auditory effective connectivity with these VLPFC and MTL regions. AC, auditory cortex; Brodmann areas 44 and 45; FOP, frontal operculum; HC, hippocampus; latHG, lateral Heschl’s gyrus; medHG, medial Heschl’s gyrus; MTL, medial temporal lobe; PHG, parahippocampal gyrus; VLPFC, ventro-lateral prefrontal cortex.
Figure 2
Figure 2
Macaque monkey auditory cortex electrical stimulation sites and es-fMRI results (A) Stimulation sites 1 and 2 in the right hemisphere auditory cortex in the two macaques (M1 and M2), overlaid on fMRI tonotopic parcellation of auditory cortex (see STAR methods). (B) Illustrated es-fMRI paradigm timing, not to scale. (C and D) Macaque es-fMRI group results showing significantly activated voxels during auditory cortex stimulation relative to no-stimulation trials: site 1 (C) and site 2 (D); cluster-corrected p < 0.05; Z > 2.8 (see Table S1 for list of activated anatomical regions). Results projected to the surface-rendered macaque template brain are shown. PFC, prefrontal cortex.
Figure 3
Figure 3
Human auditory cortex electrical stimulation sites and es-fMRI results (A) Stimulation of depth electrodes in the transverse temporal gyrus (Heschl’s gyrus [HG]). Human auditory cortex stimulation sites 1 and 2 are shown, looking down on the superior temporal plane. Stimulation sites are identified at the center of the adjacent contacts used for stimulation (Figure S2A shows actual contact locations in each subject). (B) es-fMRI paradigm timing. (C and D) Human es-fMRI group results shown as significantly activated voxels during stimulation relative to no-stimulation trials (cluster corrected; T = 2.8; p < 0.01) for site 1 (C) and site 2 (D), shown on the surface-rendered Montreal Neurological Institute human standard brain template.
Figure 4
Figure 4
Human results contrasting site 1 versus site 2 es-fMRI effects Same format as in Figures 3C and 3D, showing statistically significant (p < 0.01 cluster-corrected) effects where either site 1 (red color map) or site 2 (blue color map) was stronger. The corresponding contrast in monkeys yielded no cluster-corrected differences. SMG, supramarginal gyrus; vLMC, approximate location of ventral laryngeal motor cortex within M1.
Figure 5
Figure 5
Human and macaque VLPFC and MTL connectivity profiles (A) VLPFC and MTL subregion es-fMRI effects displayed as polar plots. Shown are across scanning run peak Z values and variability (±SEM [standard error of the mean]). Top plot in (A) shows monkey results; bottom plot shows human results. (B and C) Whisker plots of VLPFC (B) and MTL (C) es-fMRI activity responses (across scanning runs, peak Z value; central mark identifies the median; edges of box are 25th and 75th percentiles; whiskers extend to extreme ends of data, not including outliers in red crosses; non-overlapping notches are significantly different at p < 0.05). Also shown are sagittal and coronal slices in each species with the anatomically localized ROIs used for the analysis. (D) Effects by response hemisphere (monkeys left, humans right). (E) Human effects by stimulated hemisphere; only right hemisphere was stimulated in the monkeys. Note that the joined lines in the polar plots are not intended to suggest a continuing pattern across ROIs, only to assist in comparison of the patterns across species (A) and hemispheres (D and E); also see the whisker plots in (B) and (C).
Figure 6
Figure 6
Human electrical tractography (A) Human HG stimulation sites and VLPFC recording electrode locations. Contacts on the right hemisphere were projected onto the left hemisphere. (B and C) Average evoked response (RMS z-scores, mean and SEM) from the recording contacts shown by medHG (B) or latHG+PT (C) sites of stimulation. (D) Frames at 5, 10, 35, and 100 ms post-electrical pulse stimulation from Video S1 (subject 423) during medHG stimulation. (E) Average neurophysiological evoked potentials in VLPFC from stimulating the HG sites, showing the peak latency (ms) for each component. Asterisks at time 0 indicate stimulus artifact. (F) VLPFC stimulation and recording in HG; same format as in (E); location of stimulation and recording contacts shown on right. (G) Stimulation of HG during recordings in hippocampus (HC, shown in red in the right panels). (H) Stimulation of HC during recordings in HG.
Figure 7
Figure 7
Human VLPFC responses to speech and conditional Granger causality interconnectivity with auditory cortex (A) Left: electrode locations across all subjects (n = 8), shown as all subjects pooled and projected onto the standard template brain. Right: time-frequency resolved responses to speech sounds (common words) are shown. Shown are single subject individual channels (left column) and group average (right column) within Heschl’s gyrus (HG), superior temporal gyrus (STG), PHG, HC, and VLPFC. Subject 429 did not have hippocampal coverage; therefore, the responses from another subject (376) are shown for this region. Below the group results, horizontal bars identify significant responses subdivided by frequency bands (thin > 2 SD; thick > 4 SD relative to the pre-word baseline variability). White ∗∗∗ symbols inset in the group plots identify significant suppression. (B) State-space conditional Granger causality (CGC) results showing directional neurophysiological interactions during speech-sound presentation. Directions of influence are shown from regions of interest (rows) to recipient regions (columns) active during speech presentation. Subthreshold (not significant) regions of time-frequency CGC were set to 0 and are masked in dark blue. Note the strong dynamic directional influences, particularly between VLPFC and auditory sites, such as HG.
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