Potential role of monkey inferior parietal neurons coding action semantic equivalences as precursors of parts of speech

Abstract

The anterior portion of the inferior parietal cortex possesses comprehensive representations of actions embedded in behavioural contexts. Mirror neurons, which respond to both self-executed and observed actions, exist in this brain region in addition to those originally found in the premotor cortex. We found that parietal mirror neurons responded differentially to identical actions embedded in different contexts. Another type of parietal mirror neuron represents an inverse and complementary property of responding equally to dissimilar actions made by itself and others for an identical purpose. Here, we propose a hypothesis that these sets of inferior parietal neurons constitute a neural basis for encoding the semantic equivalence of various actions across different agents and contexts. The neurons have mirror neuron properties, and they encoded generalization of agents, differentiation of outcomes, and categorization of actions that led to common functions. By integrating the activities of these mirror neurons with various codings, we further suggest that in the ancestral primates' brains, these various representations of meaningful action led to the gradual establishment of equivalence relations among the different types of actions, by sharing common action semantics. Such differential codings of the components of actions might represent precursors to the parts of protolanguage, such as gestural communication, which are shared among various members of a society. Finally, we suggest that the inferior parietal cortex serves as an interface between this action semantics system and other higher semantic systems, through common structures of action representation that mimic language syntax.

Figure 1.

Summary of observed and predicted properties of mirror neurons in premotor (F5, from Rizzolatti et al., 1996 and Figure 2) and inferior parietal cortex (7b, from Fogassi et al., 2005, Figure 3, and Figure 4). Each action sequence can be analysed and described by agents (X, Y, general form in “S”, like subject), action forms (A, B, general form in “V”, like verb), goal of action (objects, general form in “O”), and other variables (others, general form in “Ot”). These elements are expressed in symbols as shown in the “Coding” column. In this column, “*” denotes compatibility with any substitutes. Elements in parentheses indicate that these must be specific, not compatible with any substitutes. Possible “Neuro-cognitive processes” are proposed in the rightmost column. The bottom row depicts our predictions based on these results, suggesting that when mirror neurons with five different properties are integrated into a system, the “Equivalence relations” will emerge in the brain to produce a human-like flexible linguistic system.

Figure 2.

Generalization process of action understandings. A: A representative example of inferior parietal neurons whose response patterns resemble those of classical mirror neurons in the F5 premotor cortex. Neural discharge in raster plots (top of the graph) and histograms showing numbers of spikes occurring per 100 ms bin (ordinate) are shown along the time axis (abscissa). Behavioural events were examined frame by frame (30 frames per second). This format is identical for all neural activity graphs in Figures 2–4. In this condition, the experimenter reached into the container, which sat in front of the monkey on the table, picked up the reward with his or her fingers and handed it to the monkey, which then grabbed the food, brought it to its mouth and ate it. This neuron discharged both when the monkey observed the experimenter picking up a piece of food with a precision grip (red bars under the abscissa, and red circle in the inset) and when the monkey picked up food in the same manner (blue underline and circle). B: Neural recording sites. Data from four hemispheres of three monkeys are projected onto the right parietal area (area shown by the square in the inset) of one monkey, normalized in relation to species-general configurations of intraparietal sulcus. cs, central sulcus; ips, intraparietal sulcus; ls, lateral sulcus. The red dot indicates the electrode tract from which the neurons depicted in A were recorded.

Figure 3.

Early processes for establishment of functional equivalence of action semantics. A: A representative example of neurons that exhibited activity similar to mirror neurons, firing equally during grip actions performed by the experimenter (using forceps, indicated by red bars under the abscissa) and by the monkeys themselves (using thumb and index finger, indicated by blue bars). They differed from classical mirror neuron properties in that they fired differently depending on the monkeys' preference of objects to grip (indicated in the graph). In this example, from the left, the experimenter used forceps to pick up and hand over the rewards to the monkey, and then he picked up three different rewards, cookies, peanuts, and raisins, one by one. This sequence was repeated twice to see replicability of the differential activities. Insets illustrate actions by the experimenter (red circle) or the monkey (blue circle). B: Neural recording sites. The red dot indicates the electrode tract from which the neurons depicted in A were recorded.

Figure 4.

Late functional equivalence process or preliminary process for establishment of stimulus equivalence among action semantics. A: A representative example of inferior parietal neurons that discharged equally to different actions embedded in the same behavioural context. In this condition, the container was sealed with a lid after the experimenter put a piece of food in it, and then handed to the monkey, which then removed the lid, grabbed the reward from inside, brought it to its mouth and ate it. This neuron discharged when the monkey observed the experimenter either opening (red bars under the abscissa, and red circle in the inset) or closing (red dashed bars under the abscissa, and red dashed circle in the inset) the container and also when the monkey opened the container (blue underline and circle). B: In this condition, the container could be opened using either of two distinct actions—by pushing a button at its base or by pulling up the lid. To teach the monkeys to push the button, the experimenter guided the monkeys' hand to push the button for several times. Then they gradually learned to push the button to get food items inside within a day. A representative example of neurons in which spontaneous discharges were inhibited equally when the monkey observed the experimenter opening the container by lifting its lid (red bars under the abscissa, and red circle in the inset) and also when the monkey pushed the lid-opening button on the device on which the container was placed (blue underline and circle). C: Neural recording sites. The red dots indicate the electrode tracts from which the neurons depicted in A and B, respectively, were recorded.