From monkey mirror neurons to primate behaviours: possible 'direct' and 'indirect' pathways

Abstract

The discovery of mirror neurons (MNs), deemed to be at the basis of action understanding, could constitute the potential solution to the 'correspondence problem' between one's own and others' action that is crucial for of imitative behaviours. However, it is still to be clarified whether, and how, several imitative phenomena, differing in terms of complexity and cognitive effort, could be explained within a unified framework based on MNs. Here we propose that MNs could differently contribute to distinct imitative behaviours by means of two anatomo-functional pathways, subjected to changes during development. A 'direct mirror pathway', directly influencing the descending motor output, would be responsible for neonatal and automatic imitation. This proposal is corroborated by some new behavioural evidences provided here. During development, the increased control of voluntary movements and the capacity to efficiently suppress automatic motor activation during action observation assign to the core MNs regions essentially perceptuo-cognitive functions. These functions would be exploited by an 'indirect mirror pathway' from the core regions of the MN system to prefrontal cortex. This latter would play a key role in parsing, storing and organizing motor representations, allowing the emergence of more efficient and complex imitative behaviours such as response facilitation and true imitation.

Figure 1.

Example of a MN responding during observation and execution of a grasping action. (a) Lateral view of the monkey brain. Shaded areas correspond to the ventral premotor area F5 and the inferior parietal area PFG in which MNs have been found. In (b) and (c), on the top is depicted the experimental condition, on the bottom the neuron discharge. (b) The monkey grasps the food. Six trials are shown for each condition. (c) The experimenter grasps the food in front of the observing monkey. Every little bar indicates a single action potential. Arrows indicate the grasping onset. Modified from di Pellegrino et al. (1992).

Figure 2.

Examples of neurons recorded with the motor and the visual task. (a) The paradigm used for the motor task and examples of three IPL motor neurons recorded during grasp-to-eat (1) and grasp-to-place (2, 3). Rasters and histograms are synchronized with the moment when the monkey touched the object to be grasped. Red bars: monkey releases the hand from the starting position. Green bars: monkey touches the container. Abscissa: time, bin = 20 ms; ordinate: discharge frequency in spikes per second (spk/s). (b) The paradigm used for the visual task and examples of three IPL mirror neurons recorded during the observation of grasp-to-eat (1) and grasp-to-place (2) done by an experimenter. Rasters and histograms are synchronized with the moment when the experimenter touched the object to be grasped. Conventions as in figure (a). Modified from Fogassi et al. (2005).

Figure 3.

Schematic view of the direct and indirect mirror pathways described in the text. Each box represents an area or an anatomo-functional circuit. In the case of MNs, the box refers to the circuit including both F5 and PFG cortical areas. In the case of motor neurons, the box labelled ‘PMc & PPC’ refers to both premotor and posterior parietal regions included in the cortical motor system. The anatomical connections and the weight of the information flow are depicted by the thickness of the arrows. (a) Direct mirror pathway. The red arrows indicate that the visual information is activating the mirror areas and that the activation of these areas have their main output on the descending motor pathways involving mainly the primary motor cortex (F1). Note that the anatomical connections between prefrontal cortical and motor and mirror areas exist although they are not fully functional (Fuster 2002). (b) Indirect mirror pathway. The activation of the mirror system has a reduced or suppressed direct influence on the primary motor cortex (black thin arrow). Its activation instead provides information (red thick arrows) about action goals and motor acts to prefrontal cortical areas (PFc) that in turn integrate it with motivational and contextual factors in order to select, organize and/or keep active the actions correspondent to the observed ones, in terms of general goal and/or the motor patterns.

Figure 4.

Neonatal imitation of tongue protrusion in a 3-day-old rhesus macaque. The two pictures are taken from a tape. (a) The gesture made by the model (open mouth) is depicted. (b) Picture taken about 270 ms after the first one. The gesture made by the model was repeated seven to eight times in a period of 20 s. (c) Latency of 1–8-day-old infant macaques to mouth opening in the MO and DISC conditions. *p<0.05. (d) Averaged scores (difference in frequency between stimulus period and baseline) ± s.e.m. of infant macaques responding to lip-smacking gesture tested on different postpartum days. Infant macaques have been categorized into two groups, imitators and non-imitators, according to their consistent imitative lip-smacking response towards the model on different testing days. Modified from Ferrari et al. (in press). Black bars, imitators; grey bars, non-imitators. (e) The frequency scores of infant macaques reaching and grasping obtained during neurobehavioural assessment in the first month of life. Infants have been assigned to one of the two categories (imitators/non-imitators) according to their consistent imitative responses to lip-smacking during the first week of life. Modified from Ferrari et al. (in press). Black circles, imitators; grey diamonds, non-imitators.