First-pass selectivity for semantic categories in human anteroventral temporal lobe

Abstract

How the brain encodes the semantic concepts represented by words is a fundamental question in cognitive neuroscience. Hemodynamic neuroimaging studies have robustly shown that different areas of posteroventral temporal lobe are selectively activated by images of animals versus manmade objects. Selective responses in these areas to words representing animals versus objects are sometimes also seen, but they are task-dependent, suggesting that posteroventral temporal cortex may encode visual categories, while more anterior areas encode semantic categories. Here, using the spatiotemporal resolution provided by intracranial macroelectrode and microelectrode arrays, we report category-selective responses to words representing animals and objects in human anteroventral temporal areas including inferotemporal, perirhinal, and entorhinal cortices. This selectivity generalizes across tasks and sensory modalities, suggesting that it represents abstract lexicosemantic categories. Significant category-specific responses are found in measures sensitive to synaptic activity (local field potentials, high gamma power, current sources and sinks) and unit-firing (multiunit and single-unit activity). Category-selective responses can occur at short latency (as early as 130 ms) in middle cortical layers and thus are extracted in the first pass of activity through the anteroventral temporal lobe. This activation may provide input to posterior areas for iconic representations when required by the task, as well as to the hippocampal formation for categorical encoding and retrieval of memories, and to the amygdala for emotional associations. More generally, these results support models in which the anteroventral temporal lobe plays a primary role in the semantic representation of words.

Figure 1.

Ventrotemporal category specificity in averaged local field potentials. Center, Depth electrode coordinates from all patients in Talairach space plotted on the Freesurfer average surface. Blue circles indicate electrodes at temporal recording sites demonstrating significant averaged LFP differences, gray circles indicate electrodes at temporal recording sites without significant LFP differences, and yellow cirlces indicate Talairach coordinates of either the center or maximally significant voxel for category-specific fMRI or PET responses as reported in previous literature. Coronal MRI slices of the temporal lobe are shown for each significant electrode location. Side plots, Averaged LFP waveforms (solid lines) or gamma power (dashed lines) for animals (blue) versus objects (red). Electrodes in occipitotemporal sulcus, collateral sulcus, and hippocampus/parahippocampal gyrus demonstrate category specificity. Differences are seen largely starting at 400 ms and in some cases, remain until 1500 ms after stimulus onset. In four subjects, gamma-band power (30–100 Hz) was differentially modulated by animals and objects. Latencies of significant differences are seen as early as 300 ms and as late as 1200 ms.

Figure 2.

Laminar microelectrode recordings demonstrate category-selective responses. CSD and MUA show category-specific differences between animals and manmade objects for the three implanted patients. CSD was computed as the second spatial derivative of laminar recordings. In CSD plots, outlined regions indicated statistically significant differences between animals and objects for the SZ task, or animals (ani), objects (obj), and abstract nouns (abs) in the WM or DI tasks (p < 0.05). Animal/object (ani-obj) plots were generated by subtracting the mean CSD for objects from the mean CSD for animals. Plots of the F-statistic from a one-way ANOVA indicate differences between three conditions (object/animal/abstract) for the WM or DI tasks. In MUA waveform plots, shaded regions indicate time-points with statistically significant differences. L1, The right (R) IT electrode shows a layer IV sink beginning at 160 ms that is modulated by semantic category in both SZ and WM tasks. L2, In the right PR electrode, the first sink occurs ∼100 ms in layers IV/V in all three tasks. Category specificity is seen in these same layers beginning as early as 150 ms. Differential MUA responses are seen in deeper layers and demonstrate animal-specific increases in firing beginning as early as 200 ms. L3, In the left (L) ER electrode, an initial layer V/VI sink is present beginning as early as 100 ms in the SZ task and ∼200 ms in the WM task. Category-selectivity is present in deeper layers at 130 ms and more superficial layers later. MUA responses for the WM task demonstrate animal-specific increases in firing.

Figure 3.

Perirhinal cortex single unit firing rates show animal/object information specificity. A, Single unit raster plot and peristimulus time histogram for a representative unit. B, Mean firing rate in five time bins for the same unit shown in A for animals (blue) and objects (red). From 0 to 300 ms, the drop in firing rate for objects is much larger than the drop in response to animals. C, Number of spikes per trial (sorted into animal and object trials) for each of eight identified units. Percentages indicate the proportion of trials with at least one spike in which the stimulus was a word associated with an animal (blue) or manmade object (red). Asterisks indicate the three units with statistically significant differences in firing between animal and objects trials (Wilcoxon rank-sum, p < 0.01).

Figure 4.

Model of lexicosemantic information flow in the temporal lobe. Visual inputs (either pictures or written words) are preprocessed by low-level occipital areas. Visual information proceeds to material-selective visual form areas in ventral occipitotemporal cortex that represent the structural information present in an image or the orthographic representation of a written word. Category-specificity is possibly seen in this area to images due to the structural differences between living and nonliving objects. This information then proceeds to anteroventral temporal cortex in which lexicosemantic associations are processed. Spoken word information proceeds along a similar pathway within the superior temporal cortices. When the particular task requires accessing visuostructural information after a written or auditory word input is perceived, feedback pathways (blue arrows) activate ventral occipitotemporal cortices.