Jakub Limanowski

Minimal Self-Models and the Free Energy Principle

The term “minimal phenomenal selfhood” (MPS) describes the basic, pre-reflective experience of being a self (Blanke and Metzinger, 2009). Theoretical accounts of the minimal self have long recognized the importance and the ambivalence of the body as both part of the physical world, and the enabling condition for being in this world (Gallagher, 2005a; Grafton, 2009). A recent account of MPS (Metzinger, 2004a) centers on the consideration that minimal selfhood emerges as the result of basic self-modeling mechanisms, thereby being founded on pre-reflective bodily processes. The free energy principle (FEP; Friston, 2010) is a novel unified theory of cortical function built upon the imperative that self-organizing systems entail hierarchical generative models of the causes of their sensory input, which are optimized by minimizing free energy as an approximation of the log-likelihood of the model. The implementation of the FEP via predictive coding mechanisms and in particular the active inference principle emphasizes the role of embodiment for predictive self-modeling, which has been appreciated in recent publications. In this review, we provide an overview of these conceptions and illustrate thereby the potential power of the FEP in explaining the mechanisms underlying minimal selfhood and its key constituents, multisensory integration, interoception, agency, perspective, and the experience of mineness. We conclude that the conceptualization of MPS can be well mapped onto a hierarchical generative model furnished by the FEP and may constitute the basis for higher-level, cognitive forms of self-referral, as well as the understanding of other minds.

Network Activity Underlying the Illusory Self-Attribution of a Dummy Arm

Neuroimaging has demonstrated that the illusory self‐attribution of body parts engages frontal and intraparietal brain areas, and recent evidence further suggests an involvement of visual body‐selective regions in the occipitotemporal cortex. However, little is known about the principles of information exchange within this network. Here, using automated congruent versus incongruent visuotactile stimulation of distinct anatomical locations on the participants right arm and a realistic dummy counterpart in an fMRI scanner, we induced an illusory self‐attribution of the dummy arm. The illusion consistently activated a left‐hemispheric network comprising ventral premotor cortex (PMv), intraparietal sulcus (IPS), and body‐selective regions of the lateral occipitotemporal cortex (LOC). Importantly, during the illusion, the functional coupling of the PMv and the IPS with the LOC increased substantially, and dynamic causal modeling revealed a significant enhancement of connections from the LOC and the secondary somatosensory cortex to the IPS. These results comply with the idea that the brains inference mechanisms rely on the hierarchical propagation of prediction error. During illusory self‐attribution, unpredicted ambiguous sensory input about ones body configuration may result in the generation of such prediction errors in visual and somatosensory areas, which may be conveyed to parietal integrative areas. Hum Brain Mapp 36:2284–2304, 2015.

Proprioceptive drift in the rubber hand illusion is intensified following 1 Hz TMS of the left EBA

The rubber hand illusion (RHI) is a paradigm used to induce an illusory feeling of owning a dummy hand through congruent multisensory stimulation. Thus, it can grant insights into how our brain represents our body as our own. Recent research has demonstrated an involvement of the extrastriate body area (EBA), an area of the brain that is typically implicated in the perception of non-face body parts, in illusory body ownership. In this experiment, we sought causal evidence for the involvement of the EBA in the RHI. Sixteen participants took part in a sham controlled, 1 Hz repetitive transcranial magnetic stimulation (rTMS) experiment. Participants received (RHI condition) or asynchronous (control) stroking and were asked to report the perceived location of their real hand, as well as the intensity and the temporal onset of experienced ownership of the dummy hand. Following rTMS of the left EBA, participants misjudged their real hand’s location significantly more toward the dummy hand during the RHI than after sham stimulation. This difference in “proprioceptive drift” provides the first causal evidence that the EBA is involved in the RHI and subsequently in body representation and further supports the view that the EBA is necessary for multimodal integration.

What can body ownership illusions tell us about minimal phenomenal selfhood

Illusions have become an invaluable tool for investigating how the sense of a body as ones own is constructed and maintained: During the rubber hand illusion (RHI, Botvinick and Cohen, 1998), congruent touch to ones hidden hand and a fake counterpart produces an illusion of feeling the touch on the fake hand and, more strikingly, an experience of the fake hand as part of ones body (Ehrsson et al., 2004; Tsakiris, 2010). The principles of the RHI paradigm have been extended to various body parts (Petkova et al., 2011), including even the face (Tsakiris, 2008; Apps et al., 2013); most notably, the RHI has been induced for the entire body (full body illusion, FBI), producing similar behavioral and neural responses (anxiety responses, ownership of the fake body, misperception of ones physical location; Ehrsson, 2007; Lenggenhager et al., 2007; Maselli and Slater, 2013). Such body ownership illusions (BOIs) have generated a substantial amount of research and invaluable insights into the mechanisms of body ownership (Tsakiris, 2010; Blanke, 2012; Moseley et al., 2012). The special importance of these illusions lies in the fact that what they manipulate—the sense of having a body—is one of the enabling conditions of minimal phenomenal selfhood (MPS, Gallagher, 2000; Blanke and Metzinger, 2009; Metzinger, 2013a). MPS is defined as the most basic possible kind of self-consciousness or self-awareness (Blanke and Metzinger, 2009; Gallagher and Zahavi, 2010), and investigating its enabling conditions may help us understand what it takes for an organism to have the experience of being a self. Nevertheless, in this paper I will argue that it is still unclear what exactly the mechanisms revealed by BOIs tell us about MPS, and that this needs to be clarified via a joint effort of phenomenological analysis and formal accounts of self-modeling. BOIs rest on the induction of some crossmodal conflict (e.g., touch seen on a fake hand but felt on ones real hand), which violates the predictions of ones body-model about the unity of ones body (Hohwy, 2007). This conflict is resolved by the brain by remapping modality-specific body part-centered reference frames onto each other (e.g., proprioception onto vision), so that the multimodal representation of the body and the space surrounding it remains coherent (Holmes and Spence, 2004; Makin et al., 2008; Tsakiris, 2010; Blanke, 2012). Thereby the spatio-temporal and anatomical constraints of BOIs (touch needs to occur simultaneously at corresponding locations and on a congruent body part in an anatomically plausible posture) suggest that multisensory input has to be compatible with a prior representation of the body (Tsakiris and Haggard, 2005; De Preester and Tsakiris, 2009; Tsakiris, 2010; Moseley et al., 2012). The brain seems to make a probabilistic either-or decision based on current sensory input under a prior body model, which during BOIs results in the replacement of the real body part by the “owned” fake body part (Longo et al., 2008; Moseley et al., 2012). And indeed, the neural mechanisms integrating multisensory information during the RHI may be similarly employed for ones real body parts (Gentile et al., 2013). When the rubber hand is threatened or injured, participants show behavioral, and neural anxiety responses similar as for ones real body part (Ehrsson et al., 2007). BOIs may even affect the regulation of ones physiological states: During illusory ownership, ones real limbs temperature may be downregulated (Moseley et al., 2008), and even the immune system may decrease “protection” of the own limb (Barnsley et al., 2011; Costantini, 2014). In sum, there is compelling evidence that BOIs interfere with the representation of ones body. Upon closer inspection, however, the fact that BOIs isolate “the various components that converge in the holistic experience of our bodies” (Maselli and Slater, 2013) may be a fundamental limitation when it comes to relating them to MPS.

Neuronal correlates of continuous manual tracking under varying visual movement feedback in a virtual reality environment

Abstract To accurately guide ones actions online, the brain predicts sensory action feedback ahead of time based on internal models, which can be updated by sensory prediction errors. The underlying operations can be experimentally investigated in sensorimotor adaptation tasks, in which moving under perturbed sensory action feedback requires internal model updates. Here we altered healthy participants’ visual hand movement feedback in a virtual reality setup, while assessing brain activity with functional magnetic resonance imaging (fMRI). Participants tracked a continually moving virtual target object with a photorealistic, three‐dimensional (3D) virtual hand controlled online via a data glove. During the continuous tracking task, the virtual hands movements (i.e., visual movement feedback) were repeatedly periodically delayed, which participants had to compensate for to maintain accurate tracking. This realistic task design allowed us to simultaneously investigate processes likely operating at several levels of the brains motor control hierarchy. FMRI revealed that the length of visual feedback delay was parametrically reflected by activity in the inferior parietal cortex and posterior temporal cortex. Unpredicted changes in visuomotor mapping (at transitions from synchronous to delayed visual feedback periods or vice versa) activated biological motion‐sensitive regions in the lateral occipitotemporal cortex (LOTC). Activity in the posterior parietal cortex (PPC), focused on the contralateral anterior intraparietal sulcus (aIPS), correlated with tracking error, whereby this correlation was stronger in participants with higher tracking performance. Our results are in line with recent proposals of a wide‐spread cortical motor control hierarchy, where temporoparietal regions seem to evaluate visuomotor congruence and thus possibly ground a self‐attribution of movements, the LOTC likely processes early visual prediction errors, and the aIPS computes action goal errors and possibly corresponding motor corrections. Graphical abstract Figure. No Caption available.

Posterior parietal cortex evaluates visuoproprioceptive congruence based on brief visual information

To represent one’s upper limbs for action, the brain relies on a combined position estimate based on visual and proprioceptive information. Monkey neurophysiology and human brain imaging suggest that the underlying operations are implemented in a network of fronto-parietal and occipitotemporal cortical areas. Recently, a potential hierarchical arrangement of these areas has been proposed, emphasizing the posterior parietal cortex (PPC) in early multisensory comparison and integration. Here, we used functional magnetic resonance imaging (fMRI) and a virtual reality-based setup to briefly (0.5 s) present healthy human participants photorealistic virtual hands, of matching or nonmatching anatomical side, or objects at the same or a different location than their real hidden left or right hand. The inferior parietal lobe (IPL) of the left PPC showed a significant preference for congruent visuoproprioceptive hand position information. Moreover, the left body part-selective extrastriate body area (EBA; functionally localized) significantly increased its coupling with the left IPL during visuoproprioceptive congruence vs. incongruence. Our results suggest that the PPC implements early visuoproprioceptive comparison and integration processes, likely relying on information exchange with the EBA.

(Dis-)Attending to the Body

Endogenous attention is crucial and beneficial for learning, selecting, and supervising actions. However, deliberately attending to action execution usually comes at the cost of decreased smoothness and slower performance, often severely impairs normal functioning, and in the worst case may result in pathological behavior and experience as in schizophrenic hyperreflexivity. These ambiguous modulatory effects of self-directed attention have been examined on phenomenological, computational, and implementational levels of description—a recent formalization within an active inference framework aims to accommodate all of these aspects. Here, I examine the active inference account of motor control as enabled by attentional modulation based on expected precisions of prediction errors in a brain’s hierarchical generative model of the environment. The implications of active inference fit well with a range of empirical results, they resonate well with ideomotor accounts of motor control, and they also tentatively reflect many insights from phenomenological analysis of the “lived body”. Thereby a particular strength of active inference is its hierarchical account of motor control in terms of adaptive behavior driven by the imperative to maintain the organism’s states within unsurprising boundaries. Phenomena ranging from the reflex arc to intentional, goal-directed action and the experience of oneself as an embodied agent are are thus proposed to rely on the same mechanisms operating universally throughout the brain’s hierarchical generative model. However, while the explanation of movement production and sensory attenuation in terms of low-level attentional modulation is quite elegant on the active inference view, there are some questions left open by its extension to higher levels of action control and the accompanying phenomenology of for example volition, effort, or agency. I suggest that conceptual guidance from recent accounts of phenomenal self- and world-modeling may help develop active inference into an interdisciplinary framework for investigating embodied agentive self-experience.

Fronto-Parietal Brain Responses to Visuotactile Congruence in an Anatomical Reference Frame

Spatially and temporally congruent visuotactile stimulation of a fake hand together with one’s real hand may result in an illusory self-attribution of the fake hand. Although this illusion relies on a representation of the two touched body parts in external space, there is tentative evidence that, for the illusion to occur, the seen and felt touches also need to be congruent in an anatomical reference frame. We used functional magnetic resonance imaging and a somatotopical, virtual reality-based setup to isolate the neuronal basis of such a comparison. Participants’ index or little finger was synchronously touched with the index or little finger of a virtual hand, under congruent or incongruent orientations of the real and virtual hands. The left ventral premotor cortex responded significantly more strongly to visuotactile co-stimulation of the same versus different fingers of the virtual and real hand. Conversely, the left anterior intraparietal sulcus responded significantly more strongly to co-stimulation of different versus same fingers. Both responses were independent of hand orientation congruence and of spatial congruence of the visuotactile stimuli. Our results suggest that fronto-parietal areas previously associated with multisensory processing within peripersonal space and with tactile remapping evaluate the congruence of visuotactile stimulation on the body according to an anatomical reference frame.