Spontaneous eye movements reflect the representational geometries of conceptual spaces.

Functional neuroimaging studies indicate that the human brain can represent concepts and their relational structure in memory using coding schemes typical of spatial navigation. However, whether we can read out the internal representational geometries of conceptual spaces solely from human behavior remains unclear. Here, we report that the relational structure between concepts in memory might be reflected in spontaneous eye movements during verbal fluency tasks: When we asked participants to randomly generate numbers, their eye movements correlated with distances along the left-to-right one-dimensional geometry of the number space (mental number line), while they scaled with distance along the ring-like two-dimensional geometry of the color space (color wheel) when they randomly generated color names. Moreover, when participants randomly produced animal names, eye movements correlated with low-dimensional similarity in word frequencies. These results suggest that the representational geometries used to internally organize conceptual spaces might be read out from gaze behavior.

Mental search of concepts is supported by egocentric vector representations and restructured grid maps.

The human hippocampal-entorhinal system is known to represent both spatial locations and abstract concepts in memory in the form of allocentric cognitive maps. Using fMRI, we show that the human parietal cortex evokes complementary egocentric representations in conceptual spaces during goal-directed mental search, akin to those observable during physical navigation to determine where a goal is located relative to oneself (e.g., to our left or to our right). Concurrently, the strength of the grid-like signal, a neural signature of allocentric cognitive maps in entorhinal, prefrontal, and parietal cortices, is modulated as a function of goal proximity in conceptual space. These brain mechanisms might support flexible and parallel readout of where target conceptual information is stored in memory, capitalizing on complementary reference frames.

The neural representation of absolute direction during mental navigation in conceptual spaces.

When humans mentally "navigate" bidimensional uniform conceptual spaces, they recruit the same grid-like and distance codes typically evoked when exploring the physical environment. Here, using fMRI, we show evidence that conceptual navigation also elicits another kind of spatial code: that of absolute direction. This code is mostly localized in the medial parietal cortex, where its strength predicts participants' comparative semantic judgments. It may provide a complementary mechanism for conceptual navigation outside the hippocampal formation.

Symbolic categorization of novel multisensory stimuli in the human brain.

When primates (both human and non-human) learn to categorize simple visual or acoustic stimuli by means of non-verbal matching tasks, two types of changes occur in their brain: early sensory cortices increase the precision with which they encode sensory information, and parietal and lateral prefrontal cortices develop a categorical response to the stimuli. Contrary to non-human animals, however, our species mostly constructs categories using linguistic labels. Moreover, we naturally tend to define categories by means of multiple sensory features of the stimuli. Here we trained adult subjects to parse a novel audiovisual stimulus space into 4 orthogonal categories, by associating each category to a specific symbol. We then used multi-voxel pattern analysis (MVPA) to show that during a cross-format category repetition detection task three neural representational changes were detectable. First, visual and acoustic cortices increased both precision and selectivity to their preferred sensory feature, displaying increased sensory segregation. Second, a frontoparietal network developed a multisensory object-specific response. Third, the right hippocampus and, at least to some extent, the left angular gyrus, developed a shared representational code common to symbols and objects. In particular, the right hippocampus displayed the highest level of abstraction and generalization from a format to the other, and also predicted symbolic categorization performance outside the scanner. Taken together, these results indicate that when humans categorize multisensory objects by means of language the set of changes occurring in the brain only partially overlaps with that described by classical models of non-verbal unisensory categorization in primates.

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

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.

Grid-like and distance codes for representing word meaning in the human brain.

Relational information about items in memory is thought to be represented in our brain thanks to an internal comprehensive model, also referred to as a "cognitive map". In the human neuroimaging literature, two signatures of bi-dimensional cognitive maps have been reported: the grid-like code and the distance-dependent code. While these kinds of representation were previously observed during spatial navigation and, more recently, during processing of perceptual stimuli, it is still an open question whether they also underlie the representation of the most basic items of language: words. Here we taught human participants the meaning of novel words as arbitrary labels for a set of audiovisual objects varying orthogonally in size and sound. The novel words were therefore conceivable as points in a navigable 2D map of meaning. While subjects performed a word comparison task, we recorded their brain activity using functional magnetic resonance imaging (fMRI). 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 relative angular positions of words in the word space, and (ii) a distance-dependent code, in medial prefrontal, orbitofrontal, and mid-cingulate cortices, representing the Euclidean distance between words. Additionally, we found evidence that the brain also separately represents the single dimensions of word meaning: their implied size, encoded in visual areas, and their implied sound, in Heschl's gyrus/Insula. These results support the idea that the meaning of words, when they are organized along two dimensions, is represented in the human brain across multiple maps of different dimensionality. SIGNIFICANT STATEMENT: How do we represent the meaning of words and perform comparative judgements on them in our brain? According to influential theories, concepts are conceivable as points of an internal map (where distance represents similarity) that, as the physical space, can be mentally navigated. Here we use fMRI to show that when humans compare newly learnt words, they recruit a grid-like and a distance code, the same types of neural codes that, in mammals, represent relations between locations in the environment and support physical navigation between them.

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

A recent proposal posits that humans might use the same neuronal machinery to support the representation of both spatial and nonspatial information, organizing concepts and memories using spatial codes. This view predicts that the same neuronal coding schemes characterizing navigation in the physical space (tuned to distance and direction) should underlie navigation of abstract semantic spaces, even if they are categorical and labeled by symbols. We constructed an artificial semantic environment by parsing a bidimensional audiovisual object space into four labeled categories. Before and after a nonspatial symbolic categorization training, 25 adults (15 females) were presented with pseudorandom sequences of objects and words during a functional MRI session. We reasoned that subsequent presentations of stimuli (either objects or words) referring to different categories implied implicit movements in the novel semantic space, and that such movements subtended specific distances and directions. Using whole-brain fMRI adaptation and searchlight model-based representational similarity analysis, we found evidence of both distance-based and direction-based responses in brain regions typically involved in spatial navigation: the medial prefrontal cortex and the right entorhinal cortex (EHC). After training, both regions encoded the distances between concepts, making it possible to recover a faithful bidimensional representation of the semantic space directly from their multivariate activity patterns, whereas the right EHC also exhibited a periodic modulation as a function of traveled direction. Our results indicate that the brain regions and coding schemes supporting relations and movements between spatial locations in mammals are "recycled" in humans to represent a bidimensional multisensory conceptual space during a symbolic categorization task.SIGNIFICANCE STATEMENT The hippocampal formation and the medial prefrontal cortex of mammals represent the surrounding physical space by encoding distances and directions between locations. Recent works suggested that humans use the same neural machinery to organize their memories as points of an internal map of experiences. We asked whether the same brain regions and neural codes supporting spatial navigation are recruited when humans use language to organize their knowledge of the world in categorical semantic representations. Using fMRI, we show that the medial prefrontal cortex and the entorhinal portion of the hippocampal formation represent the distances and the movement directions between concepts of a novel audiovisual semantic space, and that it was possible to reconstruct, from neural data, their relationships in memory.

Remembering faces: The effects of emotional valence and temporal recency.

It is known that the longer an information has been memorized, the stronger is its memory trace, and that emotionally-valenced information is more solid than neutral one. We investigated whether the emotional content of recent information might enhance its memory, making it as familiar as information known for a long time. We compared ERPs alternately recorded in response to old and solid information from long term memory (i.e., faces of popular movie stars), to recently acquired emotional information (faces of fictional characters), and to completely new information (faces of previously unknown people). Initially participants familiarized with the fictional police dossiers of 10 victims of dramatic deaths (recent faces), twice a day for seven days before EEG recordings. Recent faces were compared with faces of movie stars and unknown faces in an old/new recognition task. N200 and FN400 responses were affected by face familiarity (with no difference between old and recent faces), while parietal late positivity (LP) was sensitive to temporal recency, being it greater to old than recent faces. Interestingly, LP amplitude was similar for old and recent own-sex faces (victims) that were therefore equally memorable. It is shown that emotional memory can overcome temporal recency thus improving memory recall.