Abstract
How subjective experience is realized in nervous systems remains one of the great challenges in the natural sciences. An answer to this question should resolve debate about which animals are capable of subjective experience. We contend that subjective experience of sensory stimuli is dependent on the brain’s awareness of its internal neural processing of these stimuli. This premise is supported by empirical evidence demonstrating that disruption to either processing streams or awareness states perturb subjective experience. Given that the brain must predict the nature of sensory stimuli, we reason that conscious awareness is itself dependent on predictions generated by hierarchically organized forward models of the organism’s internal sensory processing. The operation of these forward models requires a specialized neural architecture and hence any nervous system lacking this architecture is unable to subjectively experience sensory stimuli. This approach removes difficulties associated with extrapolations from behavioral and brain homologies typically employed in addressing whether an animal can feel. Using nociception as a model sensation, we show here that the Drosophila brain lacks the required internal neural connectivity to implement the computations required of hierarchical forward models. Consequently, we conclude that Drosophila, and those insects with similar neuroanatomy, do not subjectively experience noxious stimuli and therefore cannot feel pain.
Highlights
Where in the phylogenetic tree of life do organisms evolve as sentient creatures with subjective experience of sensory stimuli? Given that non-human animals lack the capacity for verbal report, we must resort to making inferences about the nature of their experience based upon similarities between their behavioral responses, neural architectures and neurophysiological processes and those of humans
We contend that a better strategy is, first, to identify neural computations that are necessary for subjective experience such as in the case of pain, and to determine which animals have the neural architectures necessary to execute those algorithms (Key and Brown, 2018; Brown and Key, 2021)
By pinpointing neural processing functions as biomarkers of pain, we avoid appealing to gross similarities between motor behaviors between species, and this allows us to narrow our search down to organisms capable of monitoring their own ongoing internal processes
Summary
Where in the phylogenetic tree of life do organisms evolve as sentient creatures with subjective experience of sensory stimuli? Given that non-human animals lack the capacity for verbal report, we must resort to making inferences about the nature of their experience based upon similarities between their behavioral responses, neural architectures (structures) and neurophysiological processes (functions) and those of humans. These authors noted that the brainstem and cortex were the principal brain regions in humans containing sensory maps but they concluded that the brainstem, and not the cortex, was responsible for feelings This conclusion rested heavily on Merker’s descriptions of hydranencephalic children (see section “Do Insects Really Feel With Their Analogous “Midbrain” Structures?”) and followed Damasio’s earlier conclusion that subjective experience of both vision and hearing was occurring in the midbrain tectum of these children While others do agree with the need for hierarchical processing (Boly et al, 2017), they draw the line at including the purported highest level—prefrontal cortex—in subjective experience This conclusion seems at odds with those theories advocating a role for global integration and is not supported by lesion studies, those in primates that show that the prefrontal cortex is necessary for visual subjective experience (Odegaard et al, 2017). We introduce our framework and discuss how it incorporates hierarchical processing using predictive models as the basis for subjective experience
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