Awareness and consciousness in humans and animals - neural and behavioral correlates in an evolutionary perspective

Abstract

Awareness or consciousness in the context of stimulus perception can directly be assessed in well controlled test situations with humans via the persons' reports about their subjective experiences with the stimuli. Since we have no direct access to subjective experiences in animals, their possible awareness or consciousness in stimulus perception tasks has often been inferred from behavior and cognitive abilities previously observed in aware and conscious humans. Here, we analyze published human data primarily on event-related potentials and brain-wave generation during perception and responding to sensory stimuli and extract neural markers (mainly latencies of evoked-potential peaks and of gamma-wave occurrence) indicating that a person became aware or conscious of the perceived stimulus. These neural correlates of consciousness were then applied to sets of corresponding data from various animals including several species of mammals, and one species each of birds, fish, cephalopods, and insects. We found that the neural markers from studies in humans could also successfully be applied to the mammal and bird data suggesting that species in these animal groups can become subjectively aware of and conscious about perceived stimuli. Fish, cephalopod and insect data remained inconclusive. In an evolutionary perspective we have to consider that both awareness of and consciousness about perceived stimuli appear as evolved, attention-dependent options added to the ongoing neural activities of stimulus processing and action generation. Since gamma-wave generation for functional coupling of brain areas in aware/conscious states is energetically highly cost-intensive, it remains to be shown which animal species under which conditions of lifestyle and ecological niche may achieve significant advantages in reproductive fitness by drawing upon these options. Hence, we started our discussion about awareness and consciousness in animals with the question in how far these expressions of brain activity are necessary attributes for perceiving stimuli and responding in an adaptive way.

Keywords: EEG; ERP; brain energy costs; brain waves; event-related potentials; gamma-band activity; neural correlates of consciousness; selective attention.

FIGURE 1

Event-related potentials (ERPs) in response to visual stimuli (starting at the point of origin) in human observers. (A) Potentials recorded from surface electrodes above the occipital cortex contralateral to the stimulated visual field. Red curve, correct response with high-awareness; blue curve, correct response reported without awareness; gray curve, incorrect response without awareness. The red and blue curves show significant visual awareness with peaks near 200 ms latency (N200, visual awareness negativity, VAN) after stimulus onset. In addition, the red curve shows a so called P3 (positive peak later than 300 ms after stimulus onset), which is related to a conscious response [modified from Koivisto and Grassini (2016); part of their Figure 2]. (B) Potentials recorded from surface electrodes above the left-side posterior-temporal cortex to stimuli in the center of the visual field. Red curve, high-awareness with behavioral response to relevant stimulus; purple curve, low-awareness without response to irrelevant stimulus; brown curves, looking at masked relevant (solid line) or masked irrelevant stimulus (dashed line) without response requirement. The visual awareness negativities (peaks near 200 ms latency after stimulus onset) increase with increasing visibility and relevance of the stimuli corresponding to a respective increase in the awareness of the stimuli. Only the red curve shows a broad P3-like peak in the latency range of about 350–500 ms, possibly related to the required (conscious) behavioral response [modified from Koivisto and Revonsuo (2008); their Figure 7 at T5 of the left side].

FIGURE 2

Separation of (A) awareness-related and (B) attention-related gamma-band activity when humans respond to a faint visual stimulus. Whether attended or not, a stimulus perceived with awareness induced mid-frequency gamma-band activity (about 54–64 Hz) at a latency of about 240 ms after stimulus onset (left panel). If spatial (selective) attention was directed to the stimulus, high-frequency gamma-band activity (about 76–90 Hz) occurred at a latency of about 350 ms after stimulus onset (right panel). In both panels the three stars indicate the highly significant effects in the framed areas. The brackets indicate the areas of a possible attention-related effect added to the awareness effect (left panel) or an awareness-related effect added to the attention effect (right panel). [Modified from Wyart and Tallon-Baudry (2008); their Figure 3C].

FIGURE 3

Response behavior of neurons from the crow nidopallium caudolaterale to visual stimuli in a stimulus detection task. (A) Cumulative spike rate of an example neuron responding only to a highly visible, supra-threshold stimulus with a response peak about 225 ms after stimulus onset (stimulus duration is shown by the gray area). The neurons of this response type signaled the intensity of the correct stimulus and, thus, the ability to become aware of it. (B) Cumulative spike rate of an example neuron responding in the preparation of a response to a perceived (supra-threshold or near-threshold) or allegedly perceived (false alarm) stimulus. The response was trained to be given after a 2800 ms delay from stimulus onset (dashed vertical line in A and B). Response rates in a latency window of about 380–1000 ms after stimulus onset (see arrow at 700 ms) were significantly higher when the animal responded compared to the cases when it did not respond (correct rejection or miss). The neurons of this type signaled the conscious response preparation. [Modified from Nieder et al. (2020); their Figure 2C (here Figure 3A) and Figure 2E (here Figure 3B)].

FIGURE 4

Responses of freely moving rats to a heat stimulus applied to one of the paws. (A) Averaged ERP (4 central electrodes on the rat head, 12 animals in the experimental group) in response to a heat stimulus to the right forepaw. Two negativity peaks are visible, one at about 149 ms latency after heat onset, the other at about 285 ms latency. (Modified from Peng et al., 2018; their Supplementary Figure 3). (B) EEG group response to a single heat stimulus averaged to display the gamma-band event-related synchronization (γ-ERS) for frequencies of 50–100 Hz. There are two intensity peaks of the gamma-waves, one at about 55 Hz with a 150 ms latency after heat onset, the other at about 65 Hz with a 280 ms latency. The latencies of these peaks in the gamma-band activity correspond closely to the ERP peaks shown in (A). [Modified from Peng et al. (2018); their Figure 2].

FIGURE 5

Average ERP recorded from the head of a dolphin in response to a target tone. This tone had a duration of 300 ms (horizontal line above latency axis). It was followed by a second tone signaling conditioned access to a food reward. The ERP shows a prominent negativity peaking near 200 ms latency (N200) after tone onset, and a prominent positivity around 550 ms latency (P550). [Modified from Woods et al. (1986); their Figure 3.2 response to tone #3, target tone].

FIGURE 6

ERP recorded from the central nervous system of a cuttlefish (Sepia) in response to a single light flash. The light flash had a duration of 20 ms. The ERP response showed main positivities at about 50, 75, and 100 ms latency and a negativity around 130 ms latency. [Modified from Bullock and Budelmann (1991); their Figure 2, lower part].

FIGURE 7

Global Neuronal Workspace (GNW) hypothesis for the generation of consciousness in the brain. The input arrows to the global workspace show systems (perceptual, long-term memory, evaluative, attentional) which can contribute to an interactive processing with the result of the generation of awareness of the content of stimuli and consciousness about the preparation and execution of behavior (motor systems output arrow). [Modified from Dehaene and Changeux (2011); their Figure 6, upper right panel].