Conversion of object identity to object-general semantic value in the primate temporal cortex

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Science  18 Aug 2017:
Vol. 357, Issue 6352, pp. 687-692
DOI: 10.1126/science.aan4800
  • Fig. 1 Optogenetic manipulation in macaque monkeys.

    (A) Object coding in the ventral stream. In early visual cortices, nearby neurons selectively respond to objects with similar orientation. By contrast, in the perirhinal cortex, nearby neurons selectively respond to physically dissimilar complex objects. D, dorsal; V, ventral; A, anterior; P, posterior. (B) Behavioral task. Monkeys judged whether a cue object was one of the memorized OLD objects or a trial-unique NEW object. In half of the trials, the target perirhinal region was optogenetically stimulated for 600 ms from the cue onset. Inset: Lateral view of monkey brain. (C) Cue objects and various levels of visual NEW/OLD valence (19). (D to F) Neuronal responses to cue objects. (D) Raster plot for different NEW/OLD valence levels. Left, OLD objects; right, NEW objects; gray area, cue period. (E) Peristimulus time histogram of the neuron in (D). Top, responses to the best object; middle, responses to the three best and worst OLD objects and to NEW objects (bin width, 25 ms); bottom, rank-ordered responses to OLD and NEW objects (19). (F) Population responses across valence levels (n = 10 neurons, gray lines) (19). Black lines are averages. Colors correspond to those in (E). (G) Magnetic resonance (MR) image of a brain with the glass-coated optrode penetrated. Cartoon at top shows the optogenetically transduced area (rs, rhinal sulcus; sts, superior temporal sulcus; amts, anterior-medial temporal sulcus; ots, occipital-temporal sulcus). L, lateral; M, medial. In the image, arrowheads denote electrolytic lesions for registration with histological sections (19); the dashed square is the area shown in (I) to (K). (H) In vivo fluorescence measurements along the track in (G). (I) Fluorescent histological section corresponding to (G). (J) Bright-field image of (I). (K) Nissl-stained section adjacent to (I). (L to O) Immunohistochemical staining. Yellow and white arrowheads denote ChR2-EYFP–positive and GAD67-positive neurons, respectively. Scale bars, 5 mm (G), 2 mm [(I) to (K)], 20 μm [(L) to (O)].

  • Fig. 2 Optogenetic stimulation of perirhinal neurons biases monkeys’ recognition judgment.

    (A and B) Schematic of optogenetic stimulation experiments. (A) Two optical channels were used for optogenetic stimulation as well as sham illumination to prevent the monkeys from using external cues to discriminate between stimulated and nonstimulated trials. (B) The order of stimulated and nonstimulated (sham-illuminated) trials was randomized. (C and D) Representative psychometric curves from two monkeys stimulated with 473-nm light optimal for exciting ChR2. P values show statistical significance of the horizontal shift (equi-NEW/OLD valence) and slope change in each experimental session. (E) Distribution of horizontal shifts induced by 473-nm light stimulation (n = 73 experimental sessions). Positive values show that the optogenetic stimulation biases monkeys’ judgments toward the OLD choices. Experimental sessions showing a significant horizontal shift (P < 0.05) are indicated by colored bars (19); the P value is the statistical significance of distribution shift from zero, evaluated by Wilcoxon signed-rank test. (F and G) Representative psychometric curves from two monkeys stimulated with 594-nm light. (H) Distribution of horizontal shifts induced by 594-nm light stimulation (n = 12 experimental sessions). Stimulation with 594-nm light was less effective than stimulation with 473-nm light (P = 6.05 × 10−6, Wilcoxon rank sum test).

  • Fig. 3 Relationship between neuronal activity and stimulation-induced behavioral bias.

    (A) Main panel: Scatterplot of the behavioral effects of optogenetic and electrical stimulations as a function of normalized difference in the density of OLD object–responsive neurons (DOLD) to that of NEW object–responsive neurons (DNEW) around the stimulation site (19). Blue circles, optogenetic stimulation (n = 73 experimental sessions; see also Fig. 2E); gray circles, electrical stimulation (n = 39 experimental sessions; see also fig. S7); blue and black lines, regression lines for optogenetic and electrical stimulations, respectively. The slope difference between the two regression lines was statistically significant (P = 6.68 × 10−8, interaction of analysis of covariance), indicating dissociable behavioral effects between optogenetic and electrical stimulations. Inset of the scatterplot: Mean equi-NEW/OLD valence as a function of normalized difference between DOLD and DNEW (bin width, 0.05) in optogenetic and electrical stimulations. Panels at left and right: Pairs of psychometric curves of optogenetic or electrical stimulations at the sites showing similar object-coding properties (squares and triangles). (B) Comparison of regression parameters. *P < 0.001 (difference from zero, corrected for multiple comparisons); †P < 0.05 (corrected for multiple comparisons). (C) Stimulation effects categorized according to the relative dominance of DOLD (electrical, n = 21; optogenetic, n = 47) and DNEW (electrical, n = 12; optogenetic, n = 21) (P = 1.89 × 10−6, F = 25.7, interaction of two-way ANOVA). *P < 0.05 (difference from zero, t test with Bonferroni method); †P < 0.05 (t test with Bonferroni method).

  • Fig. 4 Behavioral impacts of neuronal output from subregions of the perirhinal cortex.

    (A) Schematic for examination of behavioral impact of optogenetic or electrical stimulation on object recognition along the longitudinal axis of rostral area 36 (36r). A red arrow denotes the longitudinal axis of 36r (19). (B) Spatial distribution of the response amplitude (Max response) of recorded neurons. AP, anterior-posterior coordinate from interaural line; LM, lateral-medial coordinate from midline; gray lines, location of lip of rhinal sulcus in each hemisphere; circles and squares, location of stimulation sites in clusters 1 and 2, respectively (see fig. S11 for determination of clusters). (C) Behavioral impacts of optogenetic or electrical stimulation of each subregion within 36r (optogenetic, n = 46 and 27 experimental sessions for clusters 1 and 2; electrical, n = 17 and 22 experimental sessions for clusters 1 and 2). P values denote statistical significance evaluated by Wilcoxon signed-rank test with Bonferroni method. (D) Distribution of stimulation-induced choice bias along the longitudinal axis. The longitudinal coordinate of 0 mm was set at the location of the anterior commissure on MR images. Neuronal indices of Max response (green) and Selectivity (purple) permit comparison between changes in behavioral effects and changes in neuronal responses. *P < 0.05 (difference from zero, t test with Bonferroni method); †P < 0.05, uncorrected. Inset: Transition of relationship between behavioral impacts in electrical and optogenetic stimulation. Shown are means ± SEM of equi-NEW/OLD valence in stimulation sites, grouped along the axis. Asterisks denote significant deviation from the origin of both coordinates (95% confidence ellipse with Bonferroni method).

Supplementary Materials

  • Conversion of object identity to object-general semantic value in the primate temporal cortex

    Keita Tamura, Masaki Takeda, Rieko Setsuie, Tadashi Tsubota, Toshiyuki Hirabayashi, Kentaro Miyamoto, Yasushi Miyashita

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Materials and Methods
    • Supplementary Text
    • Figs. S1 to S14
    • References

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