Principles of Neural Design

“All brains accomplish the same core task (Sterling and Laughlin, 2015): to efficiently ensure resources for physiological systems within an animal’s body (i.”

“Maps of connectivity inform and constrain all models of how neuronal circuits transform information and subserve behavior (Braitenberg and Schüz, 1998; Marr, 1969; Sterling and Laughlin, 2015).”

“All brains accomplish the same core task (Sterling and Laughlin, 2015): to efficiently ensure resources for physiological systems within an animal’s body (i.”

“This process is called allostasis 20–22 .”

“The full biological details of the neuron are dauntingly complex [ 3 ] , but widely accepted models abstract away most of the biological detail to yield a multiple-input single-output device where a range of different mathematical formulations can be used to describe the input-out transfer…”

“Several decades of research points to a different hypothesis: the human brain has a common computational architecture that, first and foremost, supports the human body as it moves, grows, survives and reproduces [1].”

“Moreover, the brain is thought to reinstate these patterns predictively rather than reactively, to actively infer the causes of sensory inputs from the body and the world (e.g., Friston, 2010; Sterling & Laughlin, 2015; Wolpert, Diedrichsen, & Flanagan, 2011).”

“…are directly bottlenecked by the number of pixels in the camera, including the energy and time costs of transducing images from the optical to digital electronic domain, of transporting them from the sensor to the post-processor, and performing high-dimensional digital post-processing 2,23 .”

“Recently, it has been proposed that many brains within the animal kingdom are structured to function via prediction and correction (Sterling & Laughlin, 2015).”

“Not only neurons with particular information-processing tasks in the smaller nervous systems of insects, but also neurons in the neocortex of mammals exhibit an astounding diversity of genetically encoded response properties 19–21 .”

“…it is conceivable that the additional computation by local interneurons, which might be necessary to establish a combinatorial odor code, introduces metabolic costs that an insect aims to avoid whenever possible to resort to a computationally simpler labeled line (Sterling and Laughlin, 2015).”

“[4] A similar approach is taken for spikes by defining S̃j [t ](Sj [t ], Ṽj [t ])≡ Sj [t ] with associated derivatives”

“A brain implements a predictive model to regulate an organism’s body in its environment ([54,236,278,281]; see Section 2.”

“Coupling neuromorphic vision to neuromorphic processing promises low-energy and low-latency visual sensing and acting, as exhibited by agile animals such as flying insects [24].”

“stores its state (memory represented by the membrane potential and the strength of synaptic connections), and a device that performs computations (Sterling and Laughlin, 2015).”

“els discussed in the previous section. First, biological neurons possess internal dynamics on different timescales due to a plethora of bio-chemical processes that interact with the membrane dynamics [30, 65]. Because these dynamics play an important role for the approximations of the Jacobians Ht and Ft, which are th…”

“To fulfill this function the retina has to be highly organized at the cellular and tissue level to allow the visual information to be sufficiently compressed, leading to fast transmission to the brain via the optic nerve (Nassi and Callaway, 2009; Sterling and Laughlin, 2015).”

“This law is the revealed principle “send at the lowest rate” (Sterling and Laughlin, 2015).”

“In contrast, thicker fi bers are less metabolically ef fi cient but can convey more information per unit of time and are less susceptible to channel noise [72,73].”

“Cones release synaptic transmitter in darkness at the rate of a few hundred vesicles per second (31), requiring on the order of 10(4) ATPs per vesicle (5, 6) for a total of ∼2 to 3 × 10(6) ATPs/s in darkness, decreasing in the light.”

“…of the body, called allostasis (Sterling, 2012; for a discussion of some of the neuroscience hypotheses, see, e.g., Barrett, 2017b; Katsumi, Kamona et al. (2021); Katsumi, Theriault et al. (2022); Kleckner et al., 2017; Sterling & Laughlin, 2015; formodeling details, see Sennesh et al., 2022).”

“…reviewed thus far is consistent with the hypothesis that the brain’s most important job is to efficiently coordinate and regulate the systems of its body as an animal moves and grows within an ever-changing and only partly predictable external world (e.g., Ashby 1960, Sterling & Laughlin 2015).”

“The components are ‘‘irreducibly small’’ and protein circuits operate ‘‘near the thermodynamic limit of energy efficiency’’ (Sterling & Laughlin, 2015, p. 124), which is why they are used extensively in all organisms, even those with brains.”

“There are >150 identified types of neurons in just its visual periphery (the ganglia lamina, medulla and lobula) [62] and”

“One possibility is that functional interactions are described well by the concept of allostasis [1] in which activity in brainstem areas is modulated by predictions of future visceromotor fluctuations sent from limbic and paralimbic circuitry [23,127–131].”

“Cellular processes are inherently noisy—membrane potentials vacillate as, for example, ion channels flip stochastically between open and closed states, signaling molecules trigger downstream cascades, and vesicles fuse and liberate transmitter (White et al., 2000; Sterling and Laughlin, 2015).”

“Critically, an efficient brain anticipates the body’s needs and prepares the best actions to satisfy them before they arise (Sterling, 2012; Sterling & Laughlin, 2015).”

“Active inference, within this internal (forward) model, is thought to equip a brain to anticipate the needs of the body and attempt to meet those needs before they arise [52], referred to as allostasis [51], thereby allowing efficient control of purposeful motor actions in the service of a balanced energy budget.”

“…gradient in the cerebral cortex; e.g., Barbas, 2015; Hilgetag & Goulas, 2020; Margulies et al., 2016; Zhang et al., 2019), and (b) predictive regulation of the body’s energy resources, called allostasis (Schulkin & Sterling, 2019; Sennesh et al., 2021; Sterling, 2012; Sterling & Laughlin, 2015).”

“By accurately inferring causes, the brain can anticipate the needs of the body, and prepare to meet those needs before they arise (Sterling, 2012; Sterling & Laughlin, 2015).”

“For example, vision begins with a large array of photoreceptors, and hearing begins with a large array of hair cells (Sterling and Laughlin, 2015).”

“This conforms to one of Sterling & Laughlin’s [115] principles of neural design: compute intracellularly and chemically whenever possible.”

“…broad sense it does not require the existence of a conscious designer: indeed, the crucial insight of Darwinian biology is that design and function can arise from the blind, undirected, and impersonal process of natural selection (Alderson & Doyle, 2010; Dennett, 2009; Sterling & Laughlin, 2015).”

“In addition, purely reactive systems are extremely energetically inefficient (Sterling and Laughlin 2015): among other things, anticipatory dynamics enable brains to focus only on functionally significant surprises in sensory input, effectively ignoring much the incoming signal (see below).”

“…out together with the circulation of the oxygenated blood through our bodies) — functioning of this phenomenon of RSA is here hypothesized to be central to the principle of allostasis, the capacity to adjust physiological function according to predicted energy demands (Sterling & Laughlin, 2015).”

“For example, single-celled protozoans already show rather complex ingestive, defensive and reproductive behavior, which is regulated by molecular signaling (Swanson, 2012; Sterling and Laughlin, 2016).”

“Another fundamental aspect of retinal processing is the sparse and precise firing patterns of retinal ganglion cells [52], presumably due to reasons of energy efficiency [51,53].”

“Maintaining nervous tissue in a physiologically active state comes at the price of substantial energy demands (Niven, 2016; Sterling and Laughlin, 2015).”

“Decisions of the second kind involve more complex circuits that serve to detect external events, weigh their saliency and relevance, and decide when and how to act on them [1].”

“Bipolar cells may implement diffusional filtering by their dendrite positioning (Rao-Mirotznik et al., 1998; Sterling and Laughlin, 2015).”

“In section 4, we discuss the benefits of adopting the principles of neural design [43] that we demonstrated with experimental data, and in section 5 we present the concluding remarks.”

“The TCE rests on the concept of allostasis, the process by which the brain predictively regulates and balances its energy needs in service of surviving and thriving (Sterling, 2004, 2012; Sterling & Laughlin, 2015).”

“They evolved with tight metabolic constraints and the need to adapt to new environments and changing bodies, sensors, and actuators, as a result of development, gradual degradation, and wear and tear (Sterling and Laughlin, 2015).”

“…is everywhere in our bodies and brains: The rhythms by which we live include the sleep-wake circadian cycle, a steady walking gait, the pacemaker cells that keep our hearts beating, the tempo of syllables in our speech, and the oscillation of brain waves (Sterling & Laughlin, 2015; Strogatz, 2004).”

“…differences in metabolic function between humans and our closest genetic relatives, common chimpanzees (e.g., Clarke & Sokoloff, 1999), and energy regulation, including allo-stasis, is crucial to understanding evolutionary change (e.g,. Lane, 2014; Pontzer, 2015; Sterling & Laughlin, 2015).”

“…of the nervous system with respect to hyperexcit-ability is a high evolutionary price that we have to pay for the enormous computational capabilities of our energy-ef fi cient brains 292,293 , which seem to operate close to criticality that maximises information-processing 300 , but see also ref.”

“The efficient coding hypothesis suggests that the brain aims to minimize this number of necessary bits (Simoncelli & Olshausen, 2001; Srinivasan, Laughlin, & Dubs, 1982; Sterling & Laughlin, 2015).”

“Allostasis, as the continually adjustment of the body’s internal milieu to promote survival and reproduction, is a fundamental feature of the mammalian nervous system (Sterling, 2012; Sterling and Laughlin, 2015).”

“number, resulting in different speed and accuracy in nerve signaling (2, 3).”

“And in the experimental realm, energy expenditure is regarded as a major factor in animal life and behavior (Alexander, 1996), even to the small scale of a single neural action potential (Sterling and Laughlin, 2017).”

“Moreover, being able to build intelligent vision models may contribute to our understanding of the neuroscience behind visual intelligence (Sterling and Laughlin, 2015).”

“Insect brains encode efficient neural solutions matched to the animal’s neuroethological context [4].”

“The mechanisms that enable performance of these tasks can be seen at work in organisms with relatively simple nervous systems, such as the C. elegans worm (Sterling and Laughlin, 2017).”

“Less obvious but potentially equally important costs are those required for developing and maintaining the neural substrate associated with the cognitive processing and memory necessary to compare potential mates (Sterling and Laughlin 2015).”

“1 μm thin to ~10 μm thick—have major implications for their ability to transmit information (Koch et al., 2006; Perge et al., 2009, 2012; Sengupta et al., 2013; Sterling and Laughlin, 2015).”

“R approach, as she describes it, is inconsistent with the anatomic, signal processing, and metabolic properties of the brain (for a review, see Barrett, 2017, in press-b; Barrett & Simmons, 2015; Chanes & Barrett, 2016; Sterling, 2012; Sterling & Laughlin, 2015).”