Hydranencephaly (not to be confused with hydrocephaly) is a condition in which the neocortex fails to develop due to neonatal stroke, for example, whereby the space normally occupied by the cerebral hemispheres is filled with cerebrospinal fluid (Merker 2007). Hydranencephalic children have a forebrain including the hypothalamus and a brain stem upon which sits a cerebellum. Such patients can have tissue sparing at anterior and posterior cortical regions, as well as laterally at temporal cortical regions, but all cortico-cortical connections are absent[1]. Even though Merker (2007) has suggested that such children (who can survive to adulthood) are conscious, they lack all the major cognitive faculties such as fine sensorimotor control and linguistic ability. These patients, however, retain emotionality being able to smile, laugh, and cry, as well as being able to orient toward sounds or visual stimuli suggesting a functional superior colliculus, as can be exhibited by blindsight patients (Tehovnik et al. 2021). The patients can have bouts of ‘absence epilepsy’ lasting for a minute or less: after a brief seizure there is immobility, staring into space, lip smacking, eyelid fluttering, and chewing. In short, without a neocortex from birth, emotionality is expressed but consciousness involving the ability to think is severely curtailed, and an adult with complete destruction of the neocortex during adulthood is comatose and therefore not able to even display emotions (Jennett 2002).

The forgoing suggests that emotionality is mediated by subcortical networks and expressed through neocortical channels (also see Katsumi et al. 2021). This is what distinguishes us from common machines that can exhibit fine sensorimotor control as well as linguistic abilities, as evidenced by current-day robots and ChatGPT. Yet these devices lack motivation, which is a property of all biological systems programmed to survive to adulthood by fostering self-repair and to eventually replicate, a process in existence for over 500 million years, at least for multicellular organisms as started during the Cambrian explosion (Bronfman et al. 2016; Cisek 2019; Darwin 1859).

Motivational systems such as the waking-sleep cycle, feeding and energy homeostasis, drinking and osmotic homeostasis, body temperature control, and maternal and sexual behavior are regulated by the hypothalamus (Inagaki et al. 1988; Haas and Panula 2003; Mogenson 1977). And nociceptive inputs originate from the spinal cord and brain stem and are carried by A-delta- and C-fibres to innervate the sub-collicular grey matter (Ekerot et al. 1987; Gellman et al. 1983). Information about behavioral drives—namely, hedonic, appetitive, and nociceptive—are shared by the entire brain including the neocortex and the cerebellum[2][3]. As discussed, a neural transmitter that drives behavior is dopamine, which is contained in the neurons of the ventral tegmental area and substantia nigra (compacta), and which is secreted from the terminals of those neurons at the cerebellar nuclei, the neocortex, the striatum, and the hypothalamus (Berger et al. 1986, 1988; Haber and Fudge 1997; Ikai et al. 1992, 1994; Maqbool et al. 1993; Mogenson 1977; Toonen et al. 1998; Washburn et al. 2022)[4]. Moreover, the projection fields of the dopaminergic fibres overlap with the sites at which self-stimulation using electrical pulses are supported (Gallistel et al. 1981; Olds 1958; Olds and Milner 1954; Pallikaras and Shizgal 2022; Wise and Rompre 1989; Yeomans et al. 1988), and the dopaminergic pathways mediate reward and reward-seeking behavior (Berridge and Robinson 2016; Kastadinov and Hausser 2022; Ljungberg et al. 1992; Schultz et al. 1993).

Neural information, as stored in the brain, is bound together by reward. (i.e., having a goal), and this binding not only pertains to perception/ consciousness, but also to body movements; this explains why the dopaminergic projections originating from the base of the midbrain have such a broad innervation profile by which to control movement and thinking, as well as volition (Sacks 1976, 2012)[5]. On this point, Ramakrishnan, Lebedev et al. (2017) made neural recordings from the motor and somatosensory cortex (i.e., M1 and S1) of monkeys performing a center-out task with a forelimb in exchange for a liquid reward (they examined a total of 485 neurons studied in three monkeys). Up to 27% of the neurons in M1 and S1 fired in anticipation of reward delivery. Some neurons responded to a mismatch between reward anticipation and amount of reward delivered. For other neurons, a lower-than-expected reward caused increased neural firing; and still for other neurons, a higher-than-expected reward caused decreased firing. Firing about the time of the reward, differed for early versus late trials on the task. They also found licking-related cells that were modulated by licking frequency. Only a small fraction of the reward neurons discharged during licking. Accordingly, the ubiquity of the reward signal in the neocortex—and beyond (Kastadinov and Hausser 2022; Ljungberg et al. 1992; Schultz et al. 1993)—highlights the importance of reward for synchronizing behavior—and by extension, for synchronizing consciousness—toward a common goal. The observations of Ramakrishnan, Lebedev et al. (2017) concur with the anticipatory activity that exists throughout the central nervous system as previously discussed for the mouse (Hasanbegović 2024; Khilkervich, Mrsic-Flogel et al. 2024).

Furthermore, recovering from anesthesia (during which the neurons of the brain are disconnected, and consciousness eliminated)[6][7] requires that the brain undergo synaptic re-connectivity, en masse (Alkire et al. 2008). Taylor et al. (2016) has shown that optogenetic activation of the dopaminergic neurons in the ventral tegmental area during isoflurane-induced anesthesia of mice evokes EEG exhibited during wakefulness and it restores the righting reflex. Also, electrical stimulation of the ventral tegmental area (but not the substantia nigra) accelerates the emergence from isoflurane anesthesia (Solt, Brown et al. 2014). The return of the righting reflex in humans under anesthesia is correlated with the return of consciousness, and this is perhaps facilitated by D1 receptors in the hippocampus and the neocortex (Leung 2017).

Therefore, what binds perception/consciousness and behavior is reward: a freezing person will walk miles in the snow to find warmth (e.g., climbers returning from Everest to arrive at base camp), a starving, thirsty person is willing to be killed as they search for relief (e.g., folks in the Gaza Strip), fleeing a predator an individual will travel for miles and for years (e.g., Whitey Bulger fleeing from the FBI), a sexually-deprived individual will pay an extraordinary sum for a few minutes of pleasure (e.g., Donald Trump vis-à-vis Stormy Danials), and a tired sleepless person will drive well into the night until a safe place can be found for sleep (e.g., driving from New York to Miami). The hypothalamus regulates these functions (Mogenson 1977), and dopaminergic projections to the hypothalamus, the striatum, the neocortex, and the cerebellum participate in reward-related behavior (Breiter, Kahneman, Shizgal et al. 2001; Gallistel et al. 1981; Kastadinov and Hausser 2022; Pallikaras and Shizgal 2022; Olds and Milner 1954; Wise 2004; Yeomans et al. 1988). The idea that some ephemeral state detached from behavior, i.e., a consciousness with no links to perception and body movement, is surely wrong if we are to accept William James’s view that all consciousness is (eventually) expressed as a motor act (James 1890). Reward expressed through the motivational systems is what binds the behaving brain together—and low-voltage fast activity (gamma) just happens to be part of this process.

Summary

1. Emotionality is subserved by subcortical networks whose full expression is dependent on neocortical networks.

2. Current-day robots and ChatGPT lack emotionality, and they differ from biological systems in that they do not have a genetically-endowed survival instinct, a characteristic of all living organisms.

3. Motivation is mediated by subcortical circuits involving the hypothalamus for the regulation of sleep, feeding, drinking, and maternal and sexual behavior; pain, which is highly emotive, is controlled by spinal cord and brain stem pathways.

4. Dopamine is centrally involved in motivation, and the midbrain dopaminergic neurons innervate much of the brain, including the cerebellar nuclei, the neocortex, the striatum, and the hypothalamus.

5. Reward (or having a goal) is what binds together the stored information in the brain to permit a unified consciousness and behavior.

Footnotes:

[1] Cortico-cortical connections are central to consciousness (Tononi 2008).

[2] Kahneman (2011) has declared that over half of human behavior is carried out automatically. The basic drives of human beings need to be automatized so that they can devote their time to more pressing matters (Maslow 1943). The id of Freud (1899, 1940) is largely concerned with automated drives.

[3] In 2003, Nielson et al. conducted a study on the quality of dreams experienced by 1,181 university students from the universities of McGill, Trent, and Alberta in Canada (Neilson et al. 2003). The average age of the students was twenty. The most common theme was being chased or pursued with no injury (82%) and the next most common theme was sexual experience (77%). The former (i.e., being chased) was evident amongst women (83% for females vs. 78% for males) and the latter (i.e., sexual experience) was common amongst men (85% for males vs. 73% for females). Other themes reported in 50% of the subjects included falling, studying, arriving late, remembering a dead person, trying-and-trying-again, soaring through the air, failing an exam, and physical attack. Perhaps not surprising, the themes cover many of the four-F’s of evolutionary biology: fleeing, fornicating, and fighting, but (less so) of feeding (Dawkins 1976). Memories are consolidated during both slow-wave sleep and rapid eye movement sleep or dream sleep (Boyce et al. 2016; Girardeau et al. 2009; Louie and Wilson 2001; Wilson and McNaughton 1994). That the sleep state is dominated by fleeing, fornicating, and fighting [but less so by feeding: the absence of dreams of food by the students is perhaps because Western students are typically well-fed. My oldest adopted boy who experienced extreme hunger while growing up still has dreams of food and its absence] should not be surprising, given that humans like all animals must ultimately deal with the drive to survive: humans are expected to attain a population of 10 billion by the end of this century, well out-competing most other animals whose numbers are in decline [UN Report, 2019, Nature’s Dangerous Decline, May 6]. Thus, as proposed by Sigmund Freud (1899) one purpose of dreaming (a putative pathway to the id) is to remind the organism of its basic motor drives [also see Jouvet 1962, Peever et al. 2014, Porte and Hobson 1996].

[4] Dopamine is a key neurotransmitter for the mediation of motivation across both vertebrate and invertebrate species (Wise 2004; Vinauger et al. 2017).

[5] During systemic administration of L-DOPA (which potentiates dopamine levels in the neocortex) the oscillatory activity in primate V1 is enhanced within the theta range, as well as within the gamma range (Zaldivar et al. 2018).

[6] When anesthetics are administered to humans, the neocortex goes into an oscillatory state of slow-waves (e.g., delta waves, 1-3 Hz, with frequencies not surpassing 10 Hz) and the synapses of the brain are disabled by activation of GABA circuits (Attwell and Laughlin 2001; Richards 2002), preventing any form of declarative or procedural learning which depends on synaptically-connected association areas and on the execution of goal-directed body movements.

[7] The drop in energy consumption from wakefulness is greater during anesthesia than during sleep, especially for slow-wave sleep (i.e., 54% vs. 23%, Schlünzen et al. 2012).