Luca Fornia

Pain and Body Awareness: Evidence from Brain-Damaged Patients with Delusional Body Ownership

A crucial aspect for the cognitive neuroscience of pain is the interplay between pain perception and body awareness. Here we report a novel neuropsychological condition in which right brain-damaged patients displayed a selective monothematic delusion of body ownership. Specifically, when both their own and the co-experimenter’s left arms were present, these patients claimed that the latter belonged to them. We reasoned that this was an ideal condition to examine whether pain perception can be “referred” to an alien arm subjectively experienced as one’s own. Seventeen patients (11 with, 6 without the delusion), and 10 healthy controls were administered a nociceptive stimulation protocol to assess pain perception. In the OWN condition, participants placed their arms on a table in front of them. In the ALIEN condition, the co-experimenter’s left (or right) arm was placed alongside the participants’ left (or right) arm, respectively. In the OWN condition, left (or right) participants’ hand dorsum were stimulated. In the ALIEN condition, left (or right) co-experimenter’s hand dorsum was stimulated. Participants had to rate the perceived pain on a 0–5 Likert scale (0 = no pain, 5 = maximal imaginable pain). Results showed that healthy controls and patients without delusion gave scores higher than zero only when their own hands were stimulated. On the contrary, patients with delusion gave scores higher than zero both when their own hands (left or right) were stimulated and when the co-experimenter’s left hand was stimulated. Our results show that in pathological conditions, a body part of another person can become so deeply embedded in one’s own somatosensory representation to effect the subjective feeling of pain. More in general, our findings are in line with a growing number of evidence emphasizing the role of the special and unique perceptual status of body ownership in giving rise to the phenomenological experience of pain.

Somato-motor haptic processing in posterior inner perisylvian region (SII/pIC) of the macaque monkey.

The posterior inner perisylvian region including the secondary somatosensory cortex (area SII) and the adjacent region of posterior insular cortex (pIC) has been implicated in haptic processing by integrating somato-motor information during hand-manipulation, both in humans and in non-human primates. However, motor-related properties during hand-manipulation are still largely unknown. To investigate a motor-related activity in the hand region of SII/pIC, two macaque monkeys were trained to perform a hand-manipulation task, requiring 3 different grip types (precision grip, finger exploration, side grip) both in light and in dark conditions. Our results showed that 70% (n = 33/48) of task related neurons within SII/pIC were only activated during monkeys’ active hand-manipulation. Of those 33 neurons, 15 (45%) began to discharge before hand-target contact, while the remaining neurons were tonically active after contact. Thirty-percent (n = 15/48) of studied neurons responded to both passive somatosensory stimulation and to the motor task. A consistent percentage of task-related neurons in SII/pIC was selectively activated during finger exploration (FE) and precision grasping (PG) execution, suggesting they play a pivotal role in control skilled finger movements. Furthermore, hand-manipulation-related neurons also responded when visual feedback was absent in the dark. Altogether, our results suggest that somato-motor neurons in SII/pIC likely contribute to haptic processing from the initial to the final phase of grasping and object manipulation. Such motor-related activity could also provide the somato-motor binding principle enabling the translation of diachronic somatosensory inputs into a coherent image of the explored object.

The Mirror Neuron System and The Strange Case of Broca's Area

Mirror neurons, originally described in the monkey premotor area F5, are embedded in a frontoparietal network for action execution and observation. A similar Mirror Neuron System (MNS) exists in humans, including precentral gyrus, inferior parietal lobule, and superior temporal sulcus. Controversial is the inclusion of Brocas area, as homologous to F5, a relevant issue in light of the mirror hypothesis of language evolution, which postulates a key role of Brocas area in action/speech perception/production. We assess “mirror” properties of this area by combining neuroimaging and intraoperative neurophysiological techniques. Our results show that Brocas area is minimally involved in action observation and has no motor output on hand or phonoarticulatory muscles, challenging its inclusion in the MNS. The presence of these functions in premotor BA6 makes this area the likely homologue of F5 suggesting that the MNS may be involved in the representation of articulatory rather than semantic components of speech. Hum Brain Mapp 36:1010–1027, 2015.

Broca’s Area as a Pre-articulatory Phonetic Encoder: Gating the Motor Program

The exact nature of the role of Broca’s area in control of speech and whether it is exerted at the cognitive or at the motor level is still debated. Intraoperative evidence of a lack of motor responses to direct electrical stimulation (DES) of Broca’s area and the observation that its stimulation induces a “speech arrest” without an apparent effect on the ongoing activity of phono-articulatory muscles, raises the argument. Essentially, attribution of direct involvement of Broca’s area in motor control of speech, requires evidence of a functional connection of this area with the phono-articulatory muscles’ motoneurons. With a quantitative approach we investigated, in 20 patients undergoing surgery for brain tumors, whether DES delivered on Broca’s area affects the recruitment of the phono-articulatory muscles’ motor units. The electromyography (EMG) of the muscles active during two speech tasks (object picture naming and counting) was recorded during and in absence of DES on Broca’s area. Offline, the EMG of each muscle was analyzed in frequency (power spectrum, PS) and time domain (root mean square, RMS) and the two conditions compared. Results show that DES on Broca’s area induces an intensity-dependent “speech arrest.” The intensity of DES needed to induce “speech arrest” when applied on Broca’s area was higher when compared to the intensity effective on the neighboring pre-motor/motor cortices. Notably, PS and RMS measured on the EMG recorded during “speech arrest” were superimposable to those recorded at baseline. Partial interruptions of speech were not observed. Speech arrest was an “all-or-none” effect: muscle activation started only by removing DES, as if DES prevented speech onset. The same effect was observed when stimulating directly the subcortical fibers running below Broca’s area. Intraoperative data point to Broca’s area as a functional gate authorizing the phonetic translation to be executed by the motor areas. Given the absence of a direct effect on motor units recruitment, a direct control of Broca’s area on the phono-articulatory apparatus seems unlikely. Moreover, the strict correlation between DES-intensity and speech prevention, might attribute this effect to the inactivation of the subcortical fibers rather than to Broca’s cortical neurons.