Distance and Direction Codes Underlie Navigation of a Novel Semantic Space in the Human Brain

Viganò, Simone; Piazza, Manuela

doi:10.1523/jneurosci.1849-19.2020

Cited by 79 publications

(98 citation statements)

References 40 publications

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“…A recent proposal posits that this cognitive map could, in principle, support also mental navigation between abstract thoughts in humans . In a recent experiment, we had observed a directional modulation of entorhinal activity partially consistent with a grid-like code when human participants were categorizing novel audio-visual objects using words (Viganò & Piazza 2020). Due to design limitations, however, we could not conclusively demonstrate that this signal supported navigation between words solely, because participants were also processing objects in the categorization task.…”

Section: An Entorhinal Grid-like Map Of Word Meaningsmentioning

confidence: 67%

“…In the psychological literature, the mental representation of word meaning is referred to as "semantic representation". Evidence for spatial codes supporting semantic representations is still very weak: in a previous study (Viganò & Piazza 2020) we presented subjects with words and objects organized in a 2D space and we reported, using fMRI, that they evoked both a distance and a direction code (in ventromedial prefrontal and entorhinal cortex, respectively).…”

Section: Introductionmentioning

confidence: 91%

“…The peculiar firing pattern of grid cell populations can be picked up in the BOLD signal in the form of a 6-fold periodicity as a function of movement direction (Doeller et al 2010). To test this here we used Representational Similarity Analysis (RSA, Kriegeskorte et al 2008), a multivariate analytical approach that, capitalizing on the small but reliable variability in grid orientation across voxels (Doeller et al, 2010;Nau et al, 2018), has been previously successfully applied to detect a grid-like signature in the BOLD signal in entorhinal cortex (EC) and other related regions (Bellmund et al 2016;Bao et al 2019;Viganò & Piazza 2020). We started by focusing on the postero-medial EC (pmEC, Figure 2B)(see Methods), the human homologous of the rodent medial EC, where grid-cells have been originally described (Hafting et al 2005).…”

Section: A Grid-like Code In Entorhinal Cortexmentioning

confidence: 99%

“…We applied a multivariate approach (as in Bellmund et al 2016;Bao et al 2019;Viganò & Piazza 2020), here correlating the predicted grid-model to the neural dissimilarity matrix obtained from our Regions of Interest. C -Regions of Interest.…”

Section: A Grid-like Code In Entorhinal Cortexmentioning

confidence: 99%

“…Another more direct way to approach the question is to probe whether the neuronal machinery that supports spatial navigation is also involved in navigating abstract representations and whether the same types of neuronal coding schemes subtending spatial navigation are also recruited for representing and navigating among concepts in memory (Bellmund et al, 2018). Recent work has started to put this speculation to empirical test, finding grid-like and/or distance-dependent responses during navigation of 2D spaces of visual shapes (Constantinescu et al 2016;Theves et al, 2019), odours (Bao et al 2019), social hierarchies (Park, Miller, Boorman, 2019 CCN), and 2 audiovisual object categories (Viganò & Piazza 2020). While each of these studies represents one important conceptual advance in the field, they all suffer from limitations: the first is that almost all focused on one single spatial code at a time (either grid-like or distance-dependent modulations of the fMRI signal), and failed to explore other types of known spatial coding schemes (e.g., head-direction like, boundary-like, etc …).…”

Section: Introductionmentioning

confidence: 99%

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Multiple spatial codes for navigating 2-D semantic spaces

Viganò

Rubino

Soccio

et al. 2020

Preprint

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SummaryWhen mammals navigate in the physical environment, specific neurons such as grid-cells, head-direction cells, and place-cells activate to represent the navigable surface, the faced direction of movement, and the specific location the animal is visiting. Here we test the hypothesis that these codes are also activated when humans navigate abstract language-based representational spaces. Human participants learnt the meaning of novel words as arbitrary signs referring to specific artificial audiovisual objects varying in size and sound. Next, they were presented with sequences of words and asked to process them semantically while we recorded the activity of their brain using fMRI. Processing words in sequence was conceivable as movements in the semantic space, thus enabling us to systematically search for the different types of neuronal coding schemes known to represent space during navigation. By applying a combination of representational similarity and fMRI-adaptation analyses, we found evidence of i) a grid-like code in the right postero-medial entorhinal cortex, representing the general bidimensional layout of the novel semantic space; ii) a head-direction-like code in parietal cortex and striatum, representing the faced direction of movements between concepts; and iii) a place-like code in medial prefrontal, orbitofrontal, and mid cingulate cortices, representing the Euclidean distance between concepts. We also found evidence that the brain represents 1-dimensional distances between word meanings along individual sensory dimensions: implied size was encoded in secondary visual areas, and implied sound in Heschl’s gyrus/Insula. These results reveal that mentally navigating between 2D word meanings is supported by a network of brain regions hosting a variety of spatial codes, partially overlapping with those recruited for navigation in physical space.

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Section: An Entorhinal Grid-like Map Of Word Meaningsmentioning

confidence: 67%

Section: Introductionmentioning

confidence: 91%

Section: A Grid-like Code In Entorhinal Cortexmentioning

confidence: 99%

Section: A Grid-like Code In Entorhinal Cortexmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Multiple spatial codes for navigating 2-D semantic spaces

Viganò

Rubino

Soccio

et al. 2020

Preprint

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Representation of the inferred relationships in a map‐like space

Liang

Liao

et al. 2023

Human Brain Mapping

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A cognitive map is an internal representation of the external world that guides flexible behavior in a complex environment. Cognitive map theory assumes that relationships between entities can be organized using Euclidean‐based coordinates. Previous studies revealed that cognitive map theory can also be generalized to inferences about abstract spaces, such as social spaces. However, it is still unclear whether humans can construct a cognitive map by combining relational knowledge between discrete entities with multiple abstract dimensions in nonsocial spaces. Here we asked subjects to learn to navigate a novel object space defined by two feature dimensions, price and abstraction. The subjects first learned the rank relationships between objects in each feature dimension and then completed a transitive inferences task. We recorded brain activity using functional magnetic resonance imaging (fMRI) while they performed the transitive inference task. By analyzing the behavioral data, we found that the Euclidean distance between objects had a significant effect on response time (RT). The longer the one‐dimensional rank distance and two‐dimensional (2D) Euclidean distance between objects the shorter the RT. The task‐fMRI data were analyzed using both univariate analysis and representational similarity analysis. We found that the hippocampus, entorhinal cortex, and medial orbitofrontal cortex were able to represent the Euclidean distance between objects in 2D space. Our findings suggest that relationship inferences between discrete objects can be made in a 2D nonsocial space and that the neural basis of this inference is related to cognitive maps.

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The hippocampal‐entorhinal system represents nested hierarchical relations between words during concept learning

Viganò

Piazza

2021

Hippocampus

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A fundamental skill of an intelligent mind is that of being able to rapidly discover the structural organization underlying the relations across the objects or the events in the world. Humans, thanks to language, master this skill. For example, a child learning that dolphins and cats can also be referred to as mammals, not only will infer the presence of a hierarchical organization for which dolphins and cats are subordinate exemplars of the category mammals, but will also derive that dolphins are, at least at one conceptual level, more similar to cats than to sharks, despite their indisputable higher perceptual similarity to the latter. The hippocampal-entorhinal system, classically known for its involvement in relational and inferential memory, is a likely candidate to construct and hold these complex relational structures between concepts. To test this hypothesis, we trained healthy human adults to organize a novel audio-visual object space into categories labeled with novel words. Crucially, a hierarchical taxonomy existed between the object categories, and participants discovered it via inference during a simple associative object-to-word training. Using functional MRI after learning, and a combination of ROI-based multivariate analyses, we found that both the mid-anterior hippocampus and the entorhinal cortex represented the inferred hierarchical structure between words: subordinate-level words were represented more similarly to their related superordinate than to unrelated ones. This was paired, in the entorhinal cortex, by an additional signature of internalized structural representation of nested hierarchy: words referring to subordinate concepts belonging to the same superordinate category were represented more similarly compared with those not belonging to the same superordinate level: interestingly, this similarity was never directly taught to subjects nor it was made explicit during the task, but only indirectly derived through a logical inferential process and, crucially, contrasted the evidence coming from the definitional perceptual properties of the concepts. None of these results were observed before learning, when the same words were not yet semantically organized. A whole-brain searchlight revealed that the effect in the entorhinal cortex extends to a wider network of areas, encompassing the prefrontal, temporal, and parietal cortices, partially overlapping with the semantic network.

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Distance and Direction Codes Underlie Navigation of a Novel Semantic Space in the Human Brain

Cited by 79 publications

References 40 publications

Multiple spatial codes for navigating 2-D semantic spaces

Multiple spatial codes for navigating 2-D semantic spaces

Representation of the inferred relationships in a map‐like space

The hippocampal‐entorhinal system represents nested hierarchical relations between words during concept learning

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