The Social Behavior Network

Part Of: Affective Neuroscience sequence
Content Summary: 800 words, 8 min read

Primary Emotion

There are many possible emotions. How can we make sense of this diversity?

Primary emotions are often used to shed light on our emotional lives. Like primary colors, these emotions blend together to reconstitute the full spectrum of emotional experience. For example, contempt is viewed as a combination of anger and disgust.

An emotion qualifies as primary if it satisfies the following criteria:

  1. Unique Machinery. It must be localized to specific neural processes.
  2. Known Signature. A fixed set of phenomenological and behavioral expressions
  3. Universal (Pre-Cultural). Expressed in all members of a given species. For ecologically valid stimuli, response does not detract from overall fitness.
  4. Primitive (Pre-Cognitive). Activated more strenuously during early development or immediate crisis (i.e., with minimal cognitive regulation).
  5. Differentiable.  Can be dissociated from other primary emotions.

Despite consensus about the above criteria, there is less agreement on which emotions deserve membership.  Here are three representative lists.

SBN- Theories of Primary Emotions (4)

The Social Behavior Network (SBN)

Neuroscientists studying aggression have identified six brain regions that seem to produce this behavior. They are:

  1. Preoptic Area of the Hypothalamus (PO)
  2. Anterior Nucleus of the Hypothalamus (AH)
  3. Ventromedial Nucleus of the Hypothalamus (VMH)
  4. Periacquductal Gray (PAG)
  5. Lateral Septum (LS)
  6. Extended Amygdala (extAMY)

If any of these regions are damaged, an animal often becomes less aggressive. If you electrically stimulate these regions, the animal becomes enraged.

What is interesting about these six regions is that they were independently discovered by other neuroscientists who labelled them as the seat of parental care.

… AND, by yet other neuroscientists who had been investigating the neural basis of sexual behavior.

What do { Parental Care, Aggression, Sexual Behavior } have in common? They are entirely directed at members of one’s own species. These primary emotions are deeply related to animal social behavior.

Since the six nuclei { PO, AH, VMH, PAG, LS, extAMY } contribute to each of these three emotions & behaviors, they are now called the social behavior network (SBN). 

SBN- Overview

Will it turn out that all social primary emotions are created by the SBN? I don’t know. It is suggestive, however, that Play has been partially localized to the lateral septum (LS).

SBN and Emotion Selection

The SBN is one brain structure that can produce three distinct emotional response. How is this possible? How does each emotion individuate itself within a single apparatus?

To proceed, we consult our “theorizing roadmap”:

SBN- Principles of Structure Function

Conceptually, we are plagued by “too many emotions”. Thus, we can either:

  1. Examine whether our three emotions can be unified; or
  2. Look for granularity within the SBN

Since the former is impractical, let’s look more carefully at the SBN.

One way to explain emotion individuation would be a shape hypothesis. If the intensity of neuron firing is encoded by height, you might expect different topographies (landscapes) to encode different emotions. 

SBN- Emotion Differentiation Shape Hypothesis

Another hypothesis is the granularity hypothesis. This posits that there may be e.g., three subdivisions of the lateral septum, and each subdivision supports a different emotion. 

ezgif.com-crop

I tend to find this approach more plausible, given my experience with other subcortical structures. That said, time will tell. 🙂

Relation To The Basal Ganglia

The SBN is anatomically related to the basal ganglia. Recall that the basal ganglia has three loops: Associative, Sensorimotor, and Limbic. The SBN is strongly connected to, and shares two nodes with, the Limbic Loop.

SBN- SBN vs Limbic Loop (2)

As we have seen, the basal ganglia is the seat of motivation. The anatomical connection between SBN and basal ganglia mirrors the behavioral link between sociality and motivation. However, on a mathematical level, it is less clear how social emotions can be incorporated into the reinforcement learning apparatus:

SBN- Application to Neuroeconomics

Evolution of Emotion

Let’s use comparative anatomy to discover when the social behavior network evolved. By dissecting brains from five representative species, we can infer that the basal ganglia dates back to at least the origin of ray-finned fish.

SBN- Phylogeny (1)

The SBN nuclei are preserved across our representative species:

SBN- Comparative Anatomy

And hodology (connections) between SBN nuclei are preserved:

SBN- Comparative Hodology

This evidence demonstrates that the social behavior network has been around since the invention of vertebrates. It also raises important questions, such as:

  • How has the SBN changed to support hyper-social animals like primates?
  • How much further back do emotional adaptations go? Do insects feel emotions? If yes, which kinds?

Until next time.

Related Works

  • Newman (1999). The Medial Extended Amygdala in Male Reproductive Behavior: A Node in the Mammalian Social Behavior Network
  • O’connell, Hofmann (2011). The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis
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Two Cybernetic Loops

Part Of: Neuroanatomy sequence
Content Summary: 800 words, 8 min read

What Is Perception About?

Consider Aristotle’s five senses: vision, hearing, smell, touch, and taste. We know that senses are windows into physical reality. But what aspects of reality do these represent?

Vision and hearing have a special property: despite receptors being located within the body (proximal), they carry information about phenomena outside of the body (distal). They carry information about the world. In contrast, smell, touch, and taste only represent events close to the body; these encode the interaction between body and world.

This distinction is a neural primitive: the brain encodes World and Interaction in extrapersonal and peripersonal space, respectively.

However, there is a significant lacuna within this binary system: none of these concern the body. Body sensation is a crucial “sixth sense”:

twoloops-body-vs-world

Making Sense of Anatomy

We spend a lot of time discussing the nervous system. But the body houses eight other anatomical systems: reproductive, integumentary (skin), muscular, skeletal, endocrine (hormones), digestive (incl. urinary and excretory subsystems), circulatory (incl. immune and lymphatic subsystems), and respiratory.

To regulate these systems, your brain recruits the following peripheral nervous systems:

  1. Somatic, which contains spinal nerves and cranial nerves
  2. Autonomic, incl. the sympathetic “fight/flight” and parasympathetic “rest/ digest” 
  3. Neuroendocrine, incl. the HPA, HPG, HPT, and Neurohypophyseal axes
  4. Enteric, also called the “second brain”, a large mass of digestion-oriented neurons
  5. Neuroenteric, connects enteric nervous system via microbiome-gut-brain axis
  6. Neuroimmune, recently discovered, primarily mediated by glial cells
  7. Glymphatic, recently discovered, which removes metabolites via CSF during sleep
  8. Neurogaseous, recently discovered, mediated by gasotransmission

The CNS must coordinate all of these to respond to sense data and regulate anatomical systems. A complex undertaking. How might we understand such a process?

With the above trichotomy { world, interaction, body }, anatomical and sensory systems can be organized into meaningful categories:

twoloops-two-kinds-of-neural-phenomena-1

The Interlocking Loop Hypothesis posits the existence of two perception-action loops, inhabiting a gradient of abstraction:

  1. The somatic “cold” loop, world- and interaction-oriented, from exteroception to movement.
  2. The visceral “hot” loop, body-oriented, from interoception to body regulation.

Loops As Organizing Principle

Evidence for the Interlocking Loop Hypothesis comes from two anatomical principles of organisation:

First, the Bell Magendie Law is based on the observation that, in all chordates, sensory information is processed at the back of the brain, and behavioral processes are at the front (“posterior perception, anterior action”):

Cybernetics- Posterior Perception, Anterior Action

Second, the Medial Viscera Principle is the observation that visceral processes tend to reside in the center of the brain (medial regions):

two-loops-medial-viscera-principle-4

Thus we can see our loops clustering at different levels of the abstraction hierarchy.

We can also see our loops’ primary site of convergence:

Anatomically, the two loops converge on the basal ganglia, in which both somatic and visceral processes are blended to yield coherent behavior.

two-loops-intersection-at-basal-ganglia

The above quote & image are from Panksepp (1998), Affective Neuroscience.

The Basis of Motivation

Why should our two loops converge on the basal ganglia? The basal ganglia is the substrate of motivation, or “wanting”. It also participates in reinforcement learning, and its mathematical interpretation as Markov Decision Processes (MDPs).

Historically, the reward function in MDPs has proven difficult to interpret biologically; however, this task becomes straightforward on the Interlocking Loop Hypothesis. Of course the cold loop would tune its behavior to promote the hot loop’s efforts to keep the organism alive.

two-loops-motivation

The Basis of Consciousness

In Can Consciousness Be Explained?, I wrote:

Let me put forward a metaphor. Consciousness feels like the movies. More specifically, it comprises:

  1. The Mental Movie. What is the content of the movie? It includes data captured by your eyes, ears, and other senses.
  2. The Mental Subject. Who watches the movie? Only one person, with your goals and your memories – you!

On this view, to explain consciousness one must explain the origins, mechanics, and output of both Movie and Subject. (Of course, one must be careful that the Subject is not a homunculus, on pain of recursion!)

The Interlocking Loop hypothesis offers an obvious foothold in the science of consciousness:

  • The world-centric cold loop generates the Mental Movie (“a world appears”). 
  • The body-centric hot loop creates the Subject (“narrative center of gravity”)

Thus, we are no longer surprised that opioid anomalies (a visceral loop instrument) are linked to depersonalization disorders; whereas dopamine (the promoter of somatic behavior) is associated with subjective time dilation effects.

Takeaways

First, we introduced the Interlocking Loop Hypothesis:

  • Some perceptions are about the world, others are about the body.
  • The CNS is a visceral body-centric hot loop, and a somatic world-centric cold loop
  • Bell-Magendie Law: perception for both loops is posterior, action is anterior.
  • Medial Viscera Principle: hot loop is located medially, while cold loop is more lateral.

Then, we examined its implications:

  • Motivation, as generated by the basal ganglia, is loop communication software; it allows the hot loop to influence cold loop behavior.
  • Consciousness has two components: the Mental Movie and Mental Subject. These are supported by cold and hot loops, respectively.

Until next time.

Relevant Materials

  • Northoff & Panksepp (2008). The trans-species concept of self and the subcortical–cortical midline system

 

Evolution of the Basal Ganglia

Part Of: [Neuroeconomics] sequence
Followup To: [An Introduction to the Basal Ganglia]

Natural History

The Earth accreted from a protoplanetary disc 4.5 billion years ago (Ga). Geologists break up Earth’s history into four eons: the Hadeon, Archaean, Proterozoic, and Phanerozoic eons.

At 3.8 Ga, abiogenesis occurred, and the sea was awash with bacteria. Since then, there have been five major events in the history of life.

  1. At 1.85 Ga, bacterial inbreeding (symbiogenesis) led to the advent of eukaryotes, whose organelles improved cellular flexibility
  2. At 800 Ma, the advent of multicellularity: some eukaryotes discovered ways to act meaningfully in groups.
  3. At 580 Ma, animal-like adaptations, such as motility and ability to consume other living matter (heterotrophy), set off the Cambrian Explosion.
  4. At 380 Ma, some animals developed four limbs (tetrapods) and the ability to become terrestrial animals.
  5. At 320 Ma, some terrestrial animals developed mammary glands, and saw the spark of the mammals.

common-descent-natural-history

We can use the tree of life to better understand these anatomical milestones. Since all life on this planet is related (common descent), we can represent familial relations just as you would on ancestry.com. Key innovations in organism body-plans can be embedded in such graphics, as follows:

common-descent-phylogeny-milestones-2

When confronted with some biological structure, we can employ comparative anatomy to discover its origin. If an adaptation is shared across multiple species, we can infer either homology (the innovation of some common ancestor) or homoplasy (an adaptation appearing independently, a.k.a “convergent evolution”).  

For example, the spine is a homology; whereas homeothermy (warm-bloodedness) and multicellularity are homoplasies. 

Full Circuit in Vertebrates

Last time, we discussed the basal ganglia, a brain structure that is intimately involved in motivation and behavior. Here, we use comparative anatomy to discover the evolutionary origin of the basal ganglia. By dissecting brains from eight representative species, we can infer that the basal ganglia dates back to the origin of vertebrates:

bg-evolution-identifying-homology

Specifically, here are the frontal sections of the eight species. By employing sophisticated histochemistry techniques such as TH-immunostaining, we are able to directly visualize the striatal and pallidal regions of the representative basal ganglia.

bg-evolution-frontal-sections-representative-species-1This investigation was conducted by Anton Reiner in his aptly-titled 2009 paper, You cannot have a vertebrate brain without a basal ganglia. The basal ganglia is not the “reptile brain”, contra the triune brain hypothesis. It is, in fact, much older.

Ancient Subcortical Loops

One of the key structures in the midbrain is the corpora quadrigemina (Latin for “four bodies”). It is composed of bilateral expressions of the superior colliculus (SC), and the inferior colliculus (IC). Anatomically, these structures are four bumps at the posterior of the midbrain; for this reason, the corpora quadrigemina is also called the tectum (Latin for “roof”).

bg-evolution-corpora-quadrigemina

The SC receives inputs from the retina, via input from the LGN nucleus of the thalamus. The IC receives input from the auditory system, and projects to the MGN nucleus of the thalamus. For this reason, it is easy to describe these structures as a vision center, and audio center, respectively.

However, there is more to the story. SC and IC represent space topographically, and densely innervate one another. They seem to participate in coordinate transformations, which integrate multimodal sensory information. The SC and IC are actually composed of distinct anatomical regions, each of which perform specialized tasks. Importantly, the SC Deep Layer functions as a control center: basically, a predecessor of the motor cortex.

bg-evolution-corpora-quadrigemina-tectum-layers

We have seen the basal ganglia processing information from the neocortex. But the neocortex is a mammalian innovation. What did the basal ganglia do before the invention of the neocortex? If you look carefully at the basal ganglia, you can actually see afferents from the GPi / SNr / VP node into the superior colliculus (SC). It turns out that the SC drives its own loop through the basal ganglia:

basal-ganglia-subcortical-loops

The basal ganglia evolved a general-purpose reinforcement learning device, assisting behavioral computations of the superior colliculus. As motor cortex M1 began to complement and compete with the SC for motor control, it was also built on top of basal ganglia loops.

For more details, see McHaffie et al (2005). Subcortical Loops in the Basal Ganglia  

Simplified Circuit in Arthropods

Insects (arthropods) have been around long before vertebrates, evolving around the Cambrian epoch. We saw above that insects (arthropods) have a nerve cord: a predecessor of the spinal cord. Each segment of the body corresponds with a nerve bundle called a ganglia. The head segment of insects, called the cephalon, is particularly important insofar as its associated ganglia (cerebral ganglion) is the direct predecessor of the brain.

Within the cerebral ganglion, we find structures called neuropiles (analogous to modern-day nuclei) which perform specific functions:

bg-evolution-arthropod-nervous-system

One such structure (located in the protocerebrum), is the central complex (in above diagram, called the central body, CB). The central complex contains a fan-shaped body which strikingly resembles the mammalian striatum:

bg-evolution-stiatum-topography

The similarities do not stop there. The basal ganglia and central complex share homologous circuitry, and are even created by the same genetic material. In fact, we can conclude that they are the same structure, with different names. 

bg-evolution-deep-homology

Recall that the basal ganglia contains two pathways: direct and indirect. The central complex does not have an indirect pathway! This suggests that the indirect pathway evolved later, as an elaboration of more primitive motivation circuitry.

For more information, see Strausfeld & Hirth (2013). Deep Homology of Arthropod Central Complex and Vertebrate Basal Ganglia. See this response, however, for a critique.

The Evolution of Dopamine

Dopamine plays a key role in behavioral readiness. The basal ganglia contains ten times more dopamine receptors than any other brain area. When did dopamine evolve? Recall that, as a catecholamine, dopamine (DA) is heavily related to norepinephrine (NE) and epinephrine (EPI):

dopamine-catecholamine-synthesis-3

In order for these neurotransmitters to influence the nervous system, neurons must have receptors responsive to the aforementioned chemicals. Our question becomes, when did these receptors evolve?

By genomic analysis, we can confirm that DA transporters (DAT) came into existence with the invention of bilateral symmetry. This basal bilaterian also contained transporters for serotenin (SERT) and a highly flexible transporter for monoamines (MAT).

In protostomes, the MAT gene was destroyed via mutation, and replaced with the octopamine transporter (OAT). Let me repeat that. Dopamine is not used by insects etc: instead, related chemicals tyramine and octopamine (bolded above) are used in its place. 

History was not much kinder for the deuterostomes, whose dopamine transporter was destroyed. However, this clade duplicated the MAT gene to resurrect dopamine receptivity in subsequence chordates (cDAT).  

bg-evolution-biogenic-amine-evolution-1

The above analysis clearly demonstrates the volatility of natural selection, and how natural selection uses the resources at its disposal to construct neurotransmitter systems like dopamine. For more information, see Caveney et al (2006). Ancestry of neuronal monoamine transporters in the Metazoa.

Summary

  • Comparative anatomy dates the emergence of the basal ganglia to at least as early as the vertebrate clade.
  • The basal ganglia also supports the “control center” of the Deep Layer of the SC, which predates its support of neocortex.
  • Incredibly, the basal ganglia predate the brain, originated prior to arthropods (insects)! The central complex is the vertebrate basal ganglia.
  • The arthropod version of the basal ganglia does not include an indirect pathway. This innovation happened later.
  • Prior to the creation of the basal ganglia, dopamine assumed its role in promoting behavior near the invention of the core animal body-plan.

We will close by condensing these discoveries into a single graphic:

brain-evolution-milestones-4

Until next time.