4.5 The Fundamental Architecture of the Vertebrate Nervous System

The simplest neural circuits in the spinal cord of vertebrates include sensory neurons, interneurons and motor neurons which, together with their muscles, form a primordial sensory-motor circuit connecting organisms with the world in a reciprocal fashion. 

This basic architecture of the nervous system in vertebrates, including Homo sapiens, appeared in the last common ancestor of cyclostomes (jawless vertebrates including lampreys and hagfish) and gnathostomes (all other vertebrates) around 560 million years ago¹. The nervous system in vertebrates is fundamentally a tube, the neural tube, which is organised into multiple repeated segments containing the classes of neurons that form the primordial sensory-motor circuits. Towards the head, the neural tube enlarges becoming the hindbrain, midbrain and the forebrain that includes the thalamus and hypothalamus (diencephalon), and the cerebral hemispheres with cerebral cortices enclosing their subcortical cerebral nuclei (telencephalon).

Special senses appeared early in evolution, including taste, olfaction, vision, hearing and balance in parallel with central drives to maintain life, including defence reactions, temperature control, breathing, drinking, feeding and reproduction. In addition to interacting with the external world, the nervous system also senses and controls the functions of internal organs involved in blood circulation, digestion, excretion and more, primarily via autonomic neural pathways².

The relative ratio of interneurons to sensory and motor neurons increased with the evolving complexity of the nervous system, so that the evolution of the brain has been mostly associated with the growth of the number and complexity of interneurons. Thus, the human nervous system contains a few million sensory neurons, a few million motor neurons and over 70 billion interneurons (almost ten times the number of humans on earth!). These interneurons form the bulk of the brain and comprise the neural circuits that underlie the neural control of the body as well as all higher mental and cognitive functions.

The discovery of the fundamental sensory-motor architecture of the vertebrate nervous system led to the concept of ‘reflex‘ and ‘reflex arc‘ introduced at the turn of the 19^th century. According to the early physiologists, reflex responses to events of the external world seemed to be an essential component of defence and adaptation to the environment³. A full perspective of the role of the reflexes in the nervous system was eventually developed by Charles Sherrington in England in 1900⁴ and in parallel led to the principles behind the idea of conditioned reflexes developed by Ivan Pavlov in Russia in the early 20^th century.

The initial idea of a reflex arc which respond to specific external or internal stimuli was taken as evidence that all central nervous activity is generated only by sensory stimuli with no intrinsic spontaneous activity of the nervous system. This idea was consistent with the philosophical view of the brain as ‘tabula rasa’ or a ‘blank slate’ as proposed by British empiricists, John Locke and David Hume, according to whom nothing exists in the brain other than what enters via the senses⁵. 

The common definition of a reflex is that specific artificial stimuli of short duration trigger specific motor responses. For example, one of the best-known reflexes in humans is the ‘knee jerk’ whereby the quick stretch of the quadriceps (thigh) muscle, generated by tapping its tendon at the knee, activates specific sensory afferent neurons (in this case, stretch receptors) in the muscle. These make direct synaptic connections in the spinal cord with motor (efferent) neurons which cause the same muscle to contract in response. There are no interneurons in this simple two-neuron sensory-motor pathway, so it is called a monosynaptic reflex, which is present in all voluntary muscles. 

Clearly this monosynaptic reflex is not involved or activated during normal movements or walking, although information from the same sensory neurons will modify the activity of the same motor neurons during the walking cycle. In other words, walking (a form of locomotion) is not simply the result of simple reflexes but is a behaviour which involve continuous interaction of the sensory-motor loops with the terrain. Nevertheless, certain defence reactions, especially those involving escaping nociceptive (painful) stimuli, are still described as reflexes: these behaviours appear as short motor patterns in response to the harmful stimuli, such as the blink reflex in the eye or the withdrawal reflex of a limb. 

Over evolutionary time, such simple reflex neural circuits evolved into increasingly complex, species-specific, behaviours⁶. Such behaviours are part of the continuous sensory-motor interactions of organisms with the external world, an idea clearly expressed as early as 1926 by Jakob Johann von Uexküll⁷.

This perspective opens the idea to describing the sensory-motor circuits as neuromechanical loops with continuous ‘circular’ interaction between neural organisms and its environment.

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1. For discussion, see SM Suryanarayana et al (2020): The evolutionary origin of visual and somatosensory representation in the vertebrate pallium. Nature Ecology & Evolution 4, 639-651. ↩︎
2. For more see: IL Gibbins (2004): Peripheral autonomic pathways. In: G Paxinos and J K Mai (Eds.), The Human Nervous System, Second edition pp. 134-189, Elsevier Academic Press. ↩︎
3. See EC Clarke & LS Jacyna (1992): Nineteenth-Century Origins of Neuroscientific Concepts. University of California Press. ↩︎
4. See RE Burke (2007): Sir Charles Sherrington’s The integrative action of the nervous system: a centenary appreciation. Brain 10, 887-894.
   Click here for a PDF facsimile of Sherrington’s monograph: The Integrative Action of the Nervous System. (1906, Yale University Press) ↩︎
5. See Simon Cobb (2020): The Idea of the Brain: A History. Allen & Unwin. ↩︎
6. Joseph E LeDoux (2023): The Four Realms of Existence: A New Theory of Being Human. Harvard University Press. ↩︎
7. Jakob Johann von Uexküll (1926): Theoretical Biology. Harcourt Brace and Co. ↩︎