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Neural network of social interaction observation in marmosets

  1. Justine C Cléry  Is a corresponding author
  2. Yuki Hori
  3. David J Schaeffer
  4. Ravi S Menon
  5. Stefan Everling  Is a corresponding author
  1. Centre for Functional and Metabolic Mapping, Robarts Research Institute, The University of Western Ontario, Canada
  2. University of Pittsburgh, Department of Neurobiology, United States
  3. Department of Physiology and Pharmacology, The University of Western Ontario, Canada
Research Article
Cite this article as: eLife 2021;10:e65012 doi: 10.7554/eLife.65012
5 figures, 2 tables and 1 additional file

Figures

Figure 1 with 2 supplements
Group functional topology maps for social (a), social scrambled (b), nonsocial (c), and nonsocial scrambled conditions (d).

Maps are displayed on the right fiducial brain surface (lateral and medial views). The white line delineates the regions based on the atlas from Paxinos et al., 2011. The regions associated with yellow/orange scale correspond to t-scores ≥ 5.4 (p<0.001, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05). The regions associated with blue scale correspond to t-scores ≤ –5.4 (p<0.001, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05). Group maps for the left hemisphere and individual maps for both hemispheres are shown in Figure 1—figure supplement 1 and Figure 1—figure supplement 2, respectively.

Figure 1—figure supplement 1
Group functional topology maps for social (a), social scrambled (b), nonsocial (c), and nonsocial scrambled conditions (d).

Maps are displayed on the left fiducial brain surface (lateral and medial views). The white line delineates the regions based on the atlas from Paxinos et al., 2011. The regions associated with yellow/orange scale correspond to t-scores ≥ 5.4 (p<0.001, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05). The regions associated with blue scale correspond to t-scores ≤ –5.4 (p<0.001, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05).

Figure 1—figure supplement 2
Individual functional topology maps for social (a), social scrambled (b), nonsocial (c), and nonsocial scrambled conditions (d) in monkeys 1–3.

Maps are displayed on both fiducial brain surface (lateral and medial views). The white line delineates the regions based on the atlas from Paxinos et al., 2011. The regions associated with yellow/orange scale correspond to t-scores ≥ 2.3 (p<0.05, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05) for monkeys 1 and 2; and t-scores ≥ 5.4 (p<0.001, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05) for monkey 3. The regions associated with blue scale correspond to t-scores ≤ –2.3 (p<0.05, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05) for monkeys 1 and 2; and t-scores ≥ −5.4 (p<0.001, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05) for monkey 3.

Figure 2 with 2 supplements
Group functional topology comparisons between social and nonsocial conditions.

Groups maps are displayed on the right and left fiducial marmoset brain surface (lateral, medial, ventral, and dorsal views) and coronal slices. The white line delineates the regions based on the atlas from Paxinos et al., 2011. Y-coordinates are calculated with respect to the anterior commissure (in millimeters). The regions associated with yellow/orange scale correspond to t-scores ≥ 2.3 (p<0.05, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05). The regions associated with blue scale correspond to t-scores ≤ –2.3 (p<0.05, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05). Nomenclature for coronal slices is as follows: Amy/LT: amygdala/lateral temporal; CeB: cerebellum; MIP: medial intraparietal area; Nacb: nucleus accumbens; SC: superior colliculus; Tha: thalamus; VIP: ventral intraparietal area. Individual maps for both hemispheres are shown in Figure 2—figure supplement 1.

Figure 2—figure supplement 1
Individual functional topology comparisons between social and nonsocial conditions.

Individual maps are displayed on the right and left fiducial marmoset brain surface (lateral, medial, ventral, and dorsal views) for monkeys 1–3. The white line delineates the regions based on the atlas from Paxinos et al., 2011. Y-coordinates are calculated with respect to the anterior commissure (in millimeters). The regions associated with yellow/orange scale correspond to t-scores ≥ 2.3 (p<0.05, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05). The regions associated with blue scale correspond to t-scores ≤ –2.3 (p<0.05, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05).

Figure 2—figure supplement 2
Temporal signal-to-noise ratio (tSNR) map for the group data.

The group map is represented on the axial slices of the marmoset brain surface. The left hemisphere shows slightly lower tSNR than the right hemisphere. A, P, L, and R indicate anterior, posterior, left, and right orientation, respectively.

Figure 3 with 1 supplement
Group functional topology of the interaction effect [social vs. social scrambled] minus [nonsocial vs. nonsocial scrambled].

Groups maps are displayed on the right and left fiducial marmoset brain surface (lateral, medial, ventral, and dorsal views) and coronal slices. The white line delineates the regions based on the atlas from Paxinos et al., 2011. Y-coordinates are calculated with respect to the anterior commissure (in millimeters). The regions associated with yellow/orange scale correspond to t-scores ≥ 2.3 (p<0.05, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05). The regions associated with blue scale correspond to t-scores ≤ –2.3 (p<0.05, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05). Nomenclature for coronal slices is as follows: Amy/LT: amygdala/lateral temporal; CeB: cerebellum; Nacb: nucleus accumbens; SC: superior colliculus; Tha: thalamus; VIP: ventral intraparietal area. Individual maps for both hemispheres are shown in Figure 3—figure supplement 1.

Figure 3—figure supplement 1
Individual functional topology of the interaction effect [social vs. social scrambled] minus [nonsocial vs. nonsocial scrambled].

Individual maps are displayed on the right and left fiducial marmoset brain surface (lateral, medial, ventral, and dorsal views) for monkeys 1–3. The white line delineates the regions based on the atlas from Paxinos et al., 2011. Y-coordinates are calculated with respect to the anterior commissure (in millimeters). The regions associated with yellow/orange scale correspond to t-scores ≥ 2.3 (p<0.05, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05). The regions associated with blue scale correspond to t-scores ≤ –2.3 (p<0.05, AFNI’s 3dttest++, cluster-size correction from Monte Carlo simulation, α = 0.05).

The magnitude of the difference between conditions within 12 regions of interests.

These differences were calculated after extraction of the time series from these regions defined in the left and right hemisphere using the Paxinos et al., 2011 atlas and based on the group activation maps. The differences from the baseline (below each bar graph) and conditions (horizontal bars) were assessed using paired t-test, *p<0.05, **p<0.01, ***p<0.001. The error bars correspond to the standard error.

Stimuli and task-based functional magnetic resonance imaging block design.

Social condition videos, nonsocial condition videos, and their scrambled versions were displayed in a screen during task conditions blocks (12 s each) and separated by baseline blocks where a central dot was displayed in the center of the screen (18 s each). A gray background was displayed behind the dot and videos through the sequence.

Tables

Table 1
Detailed description of the actions in each of the 'social interaction’ condition for each order displayed, each clip within a block (two clips of 6 s) and each repetition (two repetitions) within the run.
Social interaction
Order 1Playing (roll over the other and touching the head)Grooming (one is lying down, the other one is sitting and grooming the other one's body)
Grooming (one is lying down, the other is sitting and grooming the other's head)Eating a biscuit (sharing food between a mother and her baby)
Order 2Playing in the forest (roll over the other and touching all body parts)Playing in the forest (roll over the other and touching all body parts including playful biting)
Grooming on a branch tree (one is lying down, the other one is sitting and grooming the other one's head)Fighting and catching each other
Order 3Grooming on a branch tree (one is lying down, the other one is sitting and grooming the other one's head)Fighting and catching each other
Playing (roll over the other and touching the head)Grooming (one is lying down, the other one is sitting and grooming the other one's body)
Table 2
Detailed description of the actions in each of the 'nonsocial interaction’ condition for each order displayed, each clip within a block (two clips of 6 s) and each repetition (two repetitions) within the run.
Nonsocial interaction
Order 1Exploring a camera tripodEating (mostly chewing)Eating banana peelScratching and exploring its environment
Eating lettuce while lying on a nest bedEating on a tree branchEating on a tree branchEating while sitting on a table and looking at the camera
Order 2Eating banana and other fruits, frontal face viewEating while sitting on a table and looking at the cameraExploring and looking at its handEating fruits profile view
Frontal face view before eating sweet potatoesEating bananas and visually exploringLooking backward, chasing insectsLooking backward before eating sweet potatoes
Order 3Eating lettuce while lying on in a nest bedEating on a tree branchEating on a tree branchEating while sitting on a table and looking at the camera
Frontal face view before eating sweet potatoesEating bananas and visually exploringLooking backward, chasing insectsLooking backward before eating sweet potatoes

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