Consciousness in humans and non-human animals: recent advances and future directions

Abstract

This joint article reflects the authors' personal views regarding noteworthy advances in the neuroscience of consciousness in the last 10 years, and suggests what we feel may be promising future directions. It is based on a small conference at the Samoset Resort in Rockport, Maine, USA, in July of 2012, organized by the Mind Science Foundation of San Antonio, Texas. Here, we summarize recent advances in our understanding of subjectivity in humans and other animals, including empirical, applied, technical, and conceptual insights. These include the evidence for the importance of fronto-parietal connectivity and of "top-down" processes, both of which enable information to travel across distant cortical areas effectively, as well as numerous dissociations between consciousness and cognitive functions, such as attention, in humans. In addition, we describe the development of mental imagery paradigms, which made it possible to identify covert awareness in non-responsive subjects. Non-human animal consciousness research has also witnessed substantial advances on the specific role of cortical areas and higher order thalamus for consciousness, thanks to important technological enhancements. In addition, much progress has been made in the understanding of non-vertebrate cognition relevant to possible conscious states. Finally, major advances have been made in theories of consciousness, and also in their comparison with the available evidence. Along with reviewing these findings, each author suggests future avenues for research in their field of investigation.

Keywords: animals; biotechnology; consciousness; human cognition; neuroimaging; theoretical neuroscience.

Figure 1

Level and contents of consciousness. The level of consciousness can be dissociated from behaviors that are traditionally regarded as a signs of vigilance or arousal (such as opening of eyes, command following etc.). Typically, high conscious levels are associated with an increased range of conscious contents. Whether or not high level of consciousness without any conscious contents is possible remains unclear. Adapted from Laureys (2005), courtesy of Giulio Tononi.

Figure 2

PET studies reveal hypometabolism in similar fronto-parietal areas in vegetative and anesthesia (areas in blue, left panel). Recent dynamic causal modeling studies also suggest a loss of top-down (reentrant) connectivity in fronto-parietal cortices in both vegetative state (left panel, assessed for response to auditory stimuli) and propofol anesthesia (right panel, assessed from spontaneous EEG). Adapted from Boly et al. (2011, 2012a). ^*Significant difference between conditions (corrected p < 0.05).

Figure 3

Mental imagery paradigm used to detect covert awareness in non-communicating patients. An activation of motor cortex in response to a motor imagery task instruction (“imagine playing tennis,” on the left) or an activation of parahippocampal gyrus in response to the instruction to perform a spatial navigation mental imagery task (“imagine visiting your home,” right) can be considered as evidence of response to command, and thus of the presence of awareness, in patients unresponsive at the bedside. Reproduced with permission from (Owen et al., 2006).

Figure 4

(A) A 2-by-2 factorial design for independent manipulation of top-down attention and conscious visibility of the stimulus (Watanabe et al., 2011). Subjects are asked to carry out one of two attention tasks while viewing either a visible or invisible target stimulus. At the same time, dependent variables, such as hemodynamic responses in the brain, are measured. Here, we illustrate roughly what participants perceived in each condition (not the physical stimulus) in the study by Watanabe and colleagues. Subjects either had to report the presence of a target letter when it appeared or whether they could see the target grating or not. (B) fMRI responses in V1 is strongly modulated by top-down attention but not by conscious visibility of the grating. Modified based on Figures 2, S2 (n = 7 in total) in (Watanabe et al., 2011). The data was provided by the original author. The area under the curve (7–18 s from the block onset) is normalized to the attended and visible condition. The error bar represents 95% confidence interval.

Figure 5

Examples for bistable stimuli used to investigate the neurophysiological correlates of conscious perception in monkeys.

Figure 6

Neurophysiological correlates of visual awareness measured in different studies by intracranial recordings in monkeys and humans. Color code depicts the reported percentage of sites modulated for a given signal: Single Unit/Multiunit (upper row), Local Field Potentials (LFP) (lower row) Gamma band (40–100 Hz), Alpha/Beta (8–30 Hz). Stimulus paradigms used in the depicted studies are in brackets next to the area label (see Figure 5). Unavailable information for a given area is given as white circle. Data were derived from following publications: V1-V4 (Leopold and Logothetis, ; Gail et al., ; Wilke et al., ; Maier et al., ; Keliris et al., 2010), LGN (Lehky and Maunsell, ; Wilke et al., 2009), STS/IT (Sheinberg and Logothetis, ; Kreiman et al., 2002), MT/MST (Logothetis and Schall, ; Williams et al., ; Maier et al., ; Wang et al., 2009), LIP (Williams et al., 2003), pulvinar (Wilke et al., 2009), FEF (Libedinsky and Livingstone, 2011), and LPFC (Panagiotaropoulos et al., 2012). Abbreviations: BR, Binocular Rivalry; BRFS, Binocular Rivalry Flash Suppression; GFS, Generalized Flash Suppression; SfM, Structure-from-Motion; AM, Apparent Motion Quartet.