Attention, Learning, and Memory: The VIGILANCE System
I found it surprising that Jaak Panksepp, in Affective Neuroscience: The Foundations of Human and Animal Emotions (1998), did not add VIGILANCE to his list of innate emotional systems in the brain since he does talk about what can be called vigilance functions.
If the SEEKING system engages to solve problems, to drive motivated action to find or create access to food, water, shelter, mate, or resources (see The Brain's SEEKING System), then what is the function of a VIGILANCE system if in fact, it does exist? Perhaps a VIGILANCE system analyzes information from our senses combined with past learning and memory—salience—and
thereby 1) determines threat as soon as possible, 2) takes notice of potential sources of food or water for later use, and 3) maintains watch over young offspring. We humans more often call this kind of behavior "attentiveness." We often do not think about how such behavior involves filtering through all the incoming stimuli from the environment while simultaneously choosing to focus on only those stimuli that, for now, best serve our interests. This kind of vigilance often involves switching from one activity to another, as circumstances change. When a person lacks such ability, he/she is often diagnosed with an attention-deficit disorder (ADD or ADHD).
From a broad perspective, whereas it is dopamine that primarily drives the SEEKING system, it is both norepinephrine and dopamine that drive the VIGILANCE system, while serotonin modulate these neurotransmitters (see Brain Neurotransmitters—an Introduction). It is surely not as simple as that, since other neuromodulators are certainly involved, but I frame it this way to help conceptualize the process by which we become sentient—aware and engaged with our environment. It is norepinephrine which is most associated with learning and attention problems in our modern-day life. In Brain Neurotransmitters—an Introduction, we discuss how neurons in the loci coerulei, a pair of structures located within the pons, synthesize norepinephrine. The pons, within the anciently evolved brain stem, is pictured below in an image courtesy of John A. Beal of Louisiana State University (image links to source). Given the location of the loci coerulei, the VIGILANCE system has been around a very long time.
The axons of neurons in the loci coerulei project throughout the entire brain. The release of norepinephrine in the neocortex is of particular concern to those who study ADD and ADHD. Amy F.T. Arnsten, in "Norepinephrine Has a Critical Modulatory Influence on Prefrontal Cortical Function"* (2000), writes: "NE [norepinephrine] cells of the locus ceruleus increase their firing in response to behaviorally relevant stimuli. Selective depletion of NE in the forebrain makes animals more distractible." Arnsten cites dysfunction in the prefrontal cortex as a fundamental component of attention-deficit hyperactivity disorder (ADHD). She points out that the prefrontal cortex "uses working memory to intelligently guide behavior, inhibiting inappropriate impulses or distractions and allowing us to plan and organize effectively." It is the neurotransmitters norepinephrine and dopamine that accomplish this attentiveness in the prefrontal cortex, explains Arnsten.
* Arnsten's article was at one time available in full on the internet. It has since been removed, however, and one is redirected to The Yale Child Study Center.
In Affective Neuroscience, Panksepp points out that many distinct emotions "share generalized components such as acetylcholine, norepinephrine, and serotonin systems for the control of attention and general arousal functions." Regarding serotonin, John Allman, in Evolving Brains (2000), emphasizes that there are at least 14 types of serotonin receptors and that "some of them came into existence long before brains first appeared about 500 million years ago." Allman explains that serotonin receptors in the brain "appear to regulate the responses of neurons to other neurotransmitters." He writes:
The axons of the serotonergic neurons project in rich profusion to every part of the central nervous system (the brain and spinal cord), where they influence the activity of virtually every neuron. This widespread influence implies that the serotonergic neurons play a fundamental role in the integration of behavior. Our sense of well-being and our capacity to organize our lives and to relate to others depend profoundly on the functional integrity of the serotonergic system.
So if we conclude that a distinct VIGILANCE system exists, it certainly involves several neurotransmitters that working together, somehow producing conscious awareness and as necessary, vigilance. That I am even trying to write about this astounds me.
But where is VIGILANCE circuitry located? Certainly, the norepinephrine pathways from the loci coerulei to all parts of the brain are part of the VIGILANCE system (see Norepinephrine action, synthesis, and pathways). But other structures and circuits are certainly involved, such as the suprachiasmatic nuclei, which control the sleep-wake cycle. These nuclei are grouped in pairs and are situated within the hypothalamus. The image to the right, illustrating how the suprachiasmatic nuclei respond to light, is from an NIH website called "The New Genetics" and links to source.
Panksepp explains that as their name implies, the suprachiasmatic nuclei lie directly behind each eye, "above the optic chiasm." Each nucleus is about the size of a grain of rice. Situated close to the optic nerve, and based on levels of incoming light, the suprachiasmatic nuclei control our circadian rhythm. The term "circadian" is Latin for "approximately a day." Panksepp writes: "Even a brief pulse of bright light given once a day will synchronize rhythms under constant 24-hour lighting conditions." He adds that influences such as caffeine and the production of melatonin can influence the function of these nuclei. Panksepp reports that neurons in the suprachiasmatic nuclei "not only maintain their firing rhythm for approximately 24 hours after being disconnected from all other brain areas but also continue to cycle for some time when removed from the body and kept in tissue culture."
Based on some of Panksepp's observations, I believe the suprachiasmatic nuclei play an important part in the SEEKING-VIGILANCE construct, a sort of operating system for the brain. He writes: "The multiple output pathways from the SCN [suprachiasmatic nuclei] control practically all behavioral rhythms that have been studied, from feeding to sleep." Panksepp explains that when both sets of nuclei are destroyed, "animals scatter their behavior rather haphazardly throughout the day instead of maintaining a cyclic routine of daily activities." The location of the suprachiasmatic nucleus within the hypothalamus is indicated in yellow in the image to the right. This image is from S.S. Nussey and S.A. Whitehead,, Endocrinology obtained from the NCBI bookshelf (links to source).
The suprachiasmatic nuclei are linked to the neurons that produce norepinephrine in the loci coerulei, within the pons portion of the brainstem. In a research summary titled "Locus Coeruleus," Gary Aston-Jones provides additional support for the idea that the
loci coerulei are part of what I call a VIGILANCE system. According to Aston-Jones, evidence indicates that the loci coerulei are "part of the arousal effector circuit from the circadian pacemaker in the suprachiasmatic nucleus." Aston-Jones explains that he and collaborators have found that suprachiasmatic nuclei and the loci coerulei are connected in a circuit via the "dorsomedial nucleus of the hypothalamus."
So we know that the suprachiasmatic nuclei are somehow interdigitated with the norepinephrine-producing neurons that innervate the entire brain, producing arousal and attentiveness while allowing for rest on a cyclical basis. Toward this point, Panksepp refers to circuitry "especially in the basal forebrain and anterior hypothalamus, from where cortical slow-wave activity can be promoted." He writes: "Repetitive electrical stimulation of these parts of the brain in awake animals readily induces sleep, and a very specific site in the ventrolateral pre-optic area has recently been identified as a potential SWS [slow-wave-sleep] generator." The pre-optic area of the hypothalamus is labeled in the illustration above.
We can be sure that a VIGILANCE system is quite more
elaborate and more difficult to delineate, however, than other circuits to which Panksepp has ascribed specific labels (i.e., SEEKING, RAGE, FEAR, PANIC/LOSS, PLAY, MATING, and CARE — see Emotions are Hard-Wired in the Brain: Introduction to Ancestral Brain Systems).
I am particularly interested in VIGILANCE mechanisms because of what are called fugues. Some definitions refer to fugues as wandering states. The New Oxford American Dictionary on my MacBook Pro provides a historical psychiatric view of fugue, stating that is is "a state or period of loss of awareness of one's identity, often coupled with flight from one's usual environment, associated with certain forms of hysteria and epilepsy."
Could it be that some of the more severe symptoms of obsessive-compulsive disorder can occur when one is in a kind of fugue, where input from the frontal cortex is not integrated with subcortical activity that is driving behavior? We will discuss such possibilities in Part 3 of MyBrainNotes.com.
Panksepp explains in Affective Neuroscience that EEG recordings clearly discriminate "three global vigilance states of the nervous system—waking, SWS [slow-wave sleep], and dreaming or REM sleep." He says that in humans, there are four stages of slow-wave sleep, during which very little "active processing" takes place in the brain. Slow-wave sleep is followed, however, with a "highly activated form of sleep" involving cortical arousal, as reflected on an EEG, even more energized than the waking state. This phase of sleep is also accompanied by rapid eye movement (REM), vivid dreaming, and muscular paralysis called atonia. Panksepp discusses how it is generally believed that slow-wave sleep "reflects ongoing bodily repair processes," while REM sleep "reflects active information reintegration within the brain."
During REM sleep, Panksepp notes that muscular twitches "break through the atonia." He writes: "During these twitches, the brain is bombarded by endogenous bolts of neural 'lightning' called PGO spikes (since they are especially evident in the visual system represented in the Pons, lateral Geniculate bodies, and Occipital cortex)." Other than the twitches during REM, the muscular atonia prevails, explains Panksepp, "because of a massive inhibition, probably induced by the amino acid transmitter glycine, exerted on the motor neurons that control the large antigravity muscles of the body."
In the illustration above left, you can see that a loud sound prompts a
PGO spike (circled in red) in the lateral geniculate of a cat during non-REM sleep. This image (links to source) is from Adrian R. Morrison, "Exploring the Neurobiology of Sleep," and is originally reproduced with permission from Acta Neurobiologiae Experimentalis from Morrison and Bowker (1975). Regarding vigilance, in Morrison's article, he tells an interesting story of how he came to understand that "the REM brain most resembles the awake brain when a person is on high alert."
Working with a cat lesioned in the area of the brain responsible for atonia, within the pons, Morrison and a student, Robert Bowker, observed that the cat flinched at an unexpected loud sound but without waking up. In other words, the cat's brain had an alerting response and since the usual atonia of REM had been disabled so to speak, the cat had a muscular reaction—a flinch. There was also an accompanying PGO spike on the EEG. Through his reading and research, since PGO spikes characterize REM sleep, Morrison has come to conclude that the alerting response is ultimately responsible for atonia. His story illustrates how he came to the conclusion that just at the moment when we are alerted to a source of danger—for example a car in our peripheral vision as we are about to cross the street—we experience a hitch in our step, a slight hesitation, what Morrison believes is a moment of atonia. And REM, he theorizes, is a long bout of alerting responses which produce atonia.
One way many animals survive in the wild is to "freeze" when they see or smell a predator in the distance so as not to attract attention with movement. Perhaps this "freezing" is the kind of atonia to which Morrison refers. On an Indiana Public Media site, in "Freeze!," Don Glass writes: "The reason an ability to freeze works as a defense is that a predator's attack behavior may actually be triggered by motion. A frog, for example, will literally starve to death in a box full of dead flies. Pass one of those flies in front of its eyes on a little string, though, and it will automatically gulp it down." Glass goes on to say "The response to freeze is completely hard-wired, so freezing shows us something about both predator and prey. Evolution has caused the freeze strategy to come into existence precisely because it fits in with the way the visual systems of predators operate."
In healthy individuals, the PGO spikes that characterize an alerting response do not occur during normal waking states. Panksepp points out, however, that in schizophrenic patients, such "electrical events have been recorded from deep limbic areas." He points out that the only other times this electrical signature has been observed during a waking state have been when a subject is "under the influence of LSD" or with complex chemical manipulations. Regarding schizophrenia, which we know somehow involves excessive dopamine transmission, Panksepp writes: "When these systems become overactive, our imagination outstrips the constraints of reality. We begin to see causality where there are only correlations."
S.M. Trbovic, in "Schizophrenia as a possible dysfunction of the suprachiasmatic nucleus" (2009), writes: "Psychosis and dreaming have many similarities, including delusions, hallucinations, bizarre thinking and perceptual distortions." Trbovic points out that schizophrenic patients "have certain sleep architecture characteristics, and distinctive biological markers suggesting abnormity of the SCN, including irregular pattern of melatonin secretion, abnormal actigraphyic studies, D1-dopamine receptors involvement in the process of entraining the SCN [suprachiasmatic nuclei] and vulnerability to psychotic exacerbation due to jet lag." It is interesting that Trbovic is interested in the role of dopamine receptors in "entraining" the suprachiasmatic nuclei since bright light normally entrains or synchronizes these structures.
Trbovic also calls attention to the influenza virus, explaining that the virus "has been implicated in the etiology of schizophrenia," and "is capable of resetting" the suprachiasmatic nuclei. Previously in MyBrainNotes.com, we discuss the role of the influenza virus in postencephalitic disorders (see Encephalitis, OCD symptoms, and Parkinsonism. In Part 3 of MyBrainNotes.com, we will discuss the role of infection in obsessive-compulsive disorder.
The image to the right depicting the stages of sleep as recorded during polysomnography is from a Department of Respiratory Care Education website, Kansas Medical Center, and links to source. Regarding norepinephrine and serotonin systems, Panksepp discusses how these systems "exhibit their highest levels of activity during waking," slow down during slow-wave sleep and "a few moments prior to REM they cease firing." He goes on to say: "In short, they are inactive during dreaming." On the other hand, other than the bursts of firing that occur when animals seek rewards, Panksepp points out that dopamine neurons fire at a steady rate throughout waking, slow-wave sleep, and REM sleep.
Panksepp explains that "prefrontal areas, which generate active plans, remain quiescent" during both slow-wave sleep and REM sleep. In contrast, "PET scan images of the brain during dreaming highlight clear arousal in the limbic system, especially the amygdala." Also, the hippocampi exhibit a highly synchronous theta rhythm during REM sleep. Panksepp notes that this type of hippocampal synchronization "is common when animals are exploring their environment" and "usually indicates that the circuits are systematically encoding information (i.e., translating recent experiences into long-term memories)." As an example, he reports that "in olfactory creatures such as rats there is a lot of whisker twitching and sniffing" during REM sleep, behaviors that are "normally seen during exploration of the environment and investigation of objects." As we discuss in The Brain's SEEKING System, it is dopamine that prompts exploratory activity. So even during sleep, the SEEKING system—running primarily on dopamine—remains ready for action.
In the previous subsection, we discuss how low serotonin levels and steady-state dopamine levels characterize the dream state. A low serotonin level "also promotes heightened emotionality, both positive and negative," writes Panksepp in Affective Neuroscience. "It is a neurochemical state that leads to impulsive behavior in humans, even ones as extreme as suicide. Probably the most striking and highly replicable neurochemical finding in the whole psychiatric literature is that individuals who have killed themselves typically have abnormally low brain serotonin activity."
With the introduction and success of drugs like Prozac, a serotonin reuptake inhibitor, we have come to better understand that low serotonin levels are associated with depressed mood. As mentioned previously, Allman explains in Evolving Brains that "serotonergic neurons play a fundamental role in the integration of behavior." Below in the blocked quotation, he cites the work of Steven Soumi and Dee Higley in explaining that low serotonin levels in individuals are also associated with increased vigilance, allowing certain individuals to serve a sort of sentinel role in their group. Perhaps continuing stressful circumstances kindle hypervigilance and somehow also decreases serotonin levels. This seems to make sense because, under the constant pressure of threat and the resulting hypervigilance required to address that threat, a person or animal would understandably become depressed and exhausted. So genetics, in providing for sentinels within groups, along with a stressful environment, may together contribute to a more sever form of depression perhaps sometimes taking shape as obsessive-compulsive disorder (OCD).
Steven Soumi and Dee Higley have suggested that animals with high serotonin levels, while more stable, are less sensitive to hazards and opportunities in the environment, which may explain why there is a diversity of serotonin levels in natural monkey populations. The low-serotonin monkeys may be the first of their group to find new food sources and may serve as sentinels that detect predators. The evolution of this increased sensitivity to environmental risks and opportunities is analogous to the evolution of specific alarm and food calls that serve to alert other group members, probably close kin sharing many genes in common, to the presence of predators or resources. Such behaviors may endanger an individual but enhance the survival of close relatives and the propagation of genes shared with the individual. The potential adaptive significance of genes for low serotonergic function may explain why mood disorders, which are associated with low serotonin levels and are typically treated by drugs that enhance the concentration of synaptic serotonin, are so prevalent in the human population.
In The Trouble With Testosterone and Other Essays on the Biology of the Human Predicament (1997), Robert M. Sapolsky writes: "People with anxiety disorders can be thought of as persistently mobilizing coping responses that are disproportionately large. For them, life is filled with threats around every corner, threats that demand a constant hypervigilance, an endless skittering search for safety, a sense that the rules are constantly changing."
Many people with disorders involving obsessions and compulsions would describe themselves as being hypervigilant, meaning they feel oversensitive to stimuli in their environment. Allman writes: "The mechanisms for vigilance that conferred a survival advantage in the evolutionary past may in some cases turn pathological in contemporary life, in which we are flooded with artificial stimuli demanding our attention."
Perhaps modern relationships, especially troubled family relationships, also contribute to hypervigilance that sometimes turns into obsessions and compulsions, especially when no acceptable outlet is available for one's emotional energy, particularly rage that must be repressed.
Working on the premise that the VIGILANCE system is inextricably linked with the SEEKING system, hypervigilance prompts SEEKING action directed towards resolving whatever danger is detected. Such coordinated action requires that the corpus striata complex coordinate dopamine neurosignaling. Over time, perhaps it is possible that hypervigilance kindles dopamine transmission—raw motivation to solve problems and quell anxiety—that subsequently co-opts symptoms from whatever influences or bioprograms that are available. When current circumstances are generally safe and secure, resulting OCD symptoms might be mild, perhaps involving cleaning or organizing. When actual circumstances are threatening and chronic, and when no acceptable outlet for hypervigilance is available, such kindled dopamine transmission might manifest in more severe symptoms such as self-directed grooming routines like trichotillomania and skin picking. We will discuss these symptoms further in Part 3 of MyBrainNotes.com.
In the following subsection, Amy F.T. Arnsten suggests that the prefrontal cortex can go "off-line" due to increased catecholamines including dopamine in the brain. This dysfunction, I think, is crucial to understanding why people with compulsions continue in behaviors that, from an objective perspective, are senseless and damaging. For lack of a better term, I call these "off-line" episodes fugues, which we briefly discuss above.
Not all children who have ADD or ADHD diagnoses have a stressful home and family environment. But some do. And then there is school. From a personal, adult perspective, I find many classrooms for young children to be exceedingly overstimulating. And I'm referring just to visual stimuli. Add in some audio and noise and stimulation increases dramatically. After school, children often return home to, you guessed it, watch television or play video games that make me dizzy. If a child is predisposed to have attention-deficit problems and/or genetically inclined, as we discuss above, to be vigilant, in my opinion, such an overabundance of stimuli is the last thing the child needs. I also think a constant overabundance of stimuli could easily produce unfocused behavior that could be misinterpreted as attention-deficit hyperactivity disorder (ADHD). It is my opinion that, especially for vulnerable children and adults, high levels of stimulation, over time, is a form of stress, even when everybody else is doing it.
"Stress Signalling Pathways That Impair Prefrontal Cortex Structure and Function", Amy F.T. Arnstem writes: "The same neurochemical events that impair prefrontal working memory abilities actually strengthen the emotional operations of the amygdala. Thus, uncontrollable stress switches control of behaviour from the thoughtful PFC to the more primitive conditioned responses of the amygdala." (See The amygdala, stress, OCD, and PTSD in Part 1 of MyBrainNotes.com.)
In Part 1 of MyBrainNotes.com, we discuss the frontal lobes in a general way and, more specifically, the orbital-frontal cortex (see The brain's frontal lobes and The orbital-frontal cortex). Now we turn our attention to what is called the prefrontal cortex, which is nicely illustrated in the image to the right (links to NIH source). Bear in mind that the prefrontal cortex includes the orbital-frontal cortex.
Regarding what she calls the prefrontal cortex, in "Stress
Impairs Prefrontal Cortical Function" (1988) Amy F.T. Arnsten writes:
Neurochemical changes in the prefrontal cortex (PFC) during periods of stress may take this brain region "off-line," making the child less able to govern his behavior.
The PFC is situated anterior to the motor cortices in the frontal lobe. It is much larger in primates than in other mammals. It continues to develop throughout adolescence. This region of our brains is critical for using "working memory," a form of memory that is required to appropriately guide behavior. Working memory has been called "scratch-pad" memory, because this type of memory must be constantly updated. Memories can be called up from long-term storage or from more recent buffers. The PFC uses these representations to effectively guide behavior, freeing us from responding only to our immediate environment, inhibiting inappropriate responses or distractions, and allowing us to plan and organize. Animals or humans with lesions to the PFC exhibit poor attention regulation, disorganized and impulsive behavior, and hyperactivity.
Arnsten succinctly explains the role of catecholamines in prefrontal cortex processing. She writes:
During stress exposure, catecholamines are released in both the peripheral and central nervous systems. In the periphery, the catecholamines norepinephrine and epinephrine are released from the sympathetic nervous system and adrenal gland, respectively. These catecholamine actions serve to "turn on" our heart and muscles and "turn off" the stomach to prepare for fight-or-flight responses during stress. In the brain, high levels of the catecholamines dopamine and norepinephrine are released in the PFC during stress exposure, even during relatively mild psychological stress. As basal levels of dopamine and norepinephrine have essential beneficial influences on PFC function, it was originally presumed that high levels of catecholamine release during stress might facilitate PFC function. However, research in monkeys and rats demonstrated the contrary: exposure to stress impairs the working memory functions of the PFC. These findings in animals are consistent with older literature demonstrating that humans exposed to loud noise stress are less able to sustain attention or to inhibit inappropriate responses, functions now known to be carried out by the PFC.
Arnsten points out that "Electrophysiological recordings similarly indicate that high levels of D1 receptor stimulation can interfere with PFC neuronal function." She explains that "Active neurochemical mechanisms to take the PFC 'off-line' during stress may have had survival value in evolution, allowing faster, instinctual mechanisms regulated by subcortical and posterior cortical areas to regulate behavior during stress. However, these brain actions may often be maladaptive in human society when we are in need of PFC regulation to act appropriately, e.g., in the classroom when behavior must be highly controlled."
The image to the right—illustrating normal brain activity during a task that activates working memory—is from an MRI connected with a supercomputer to create a three-dimensional image and links to source. It is from a webpage Pittsburgh Supercomputing Center developed titled "Watching the Brain in Action." The project's researchers include Jonathan Cohen, University of Pittsburgh and Carnegie Mellon University; Nigel Goddard, Pittsburgh Supercomputing Center; Bill Eddy, Carnegie Mellon University; and Doug Noll, University of Pittsburgh.
Based on Zahrt et al., "Supranormal Stimulation of D1 Dopamine Receptors in the Rodent Cortex Impairs Spatial Working Memory Performance" (1997), Arnsten writes: "Dopamine acting at D1 receptors in the prefrontal cortex (PFC) produces an inverted U dose response whereby either too little or too much D1 receptor stimulation impairs neuronal or cognitive function." She explains that "With insufficient D1 receptor stimulation, all signals are conveyed to the soma [nerve cell body], resulting in diffuse, unfocused information." On the other hand, with optimal levels of D1 receptor stimulation, "signal transfer is focused such that only the largest, coordinated signals are conveyed to the cell." This results in "optimal working memory and attention regulation." Arnsten writes: "At very high levels of D1 receptor stimulation such as during stress, calcium currents are blocked and signal transfer is abolished." Thus, an excessively high level of dopamine results in "poor working memory and attention regulation."
To continue exploring MyBrainNotes.com in an orderly fashion, link to Rage: an Innate Brain System.
Or, you may Explore the Site Outline.
Thanks for visiting my site. If you would like be informed about new features and improvements as they are added to MyBrainNotes.com, please send me an e-mail.