Olfactory system

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Olfactory system
Head Olfactory Nerve Labeled.png
Components of the olfactory system
Identifiers
FMA 7190
Anatomical terminology

The olfactory system, or sense of smell, is the sensory system used for olfaction (i.e., smelling). Olfaction is one of the special senses directly associated with specific organs. Most mammals and reptiles have a main olfactory system and an accessory olfactory system. The main olfactory system detects airborne substances, while the accessory system senses fluid-phase stimuli.

Contents

The senses of smell and taste (gustatory system) are often referred to together as the chemosensory system, because they both give the brain information about the chemical composition of objects through a process called transduction.

Structure

This diagram linearly (unless otherwise mentioned) tracks the projections of all known structures that allow for olfaction to their relevant endpoints in the human brain. Comprehensive List of Relevant Pathways for the Olfactory System.png
This diagram linearly (unless otherwise mentioned) tracks the projections of all known structures that allow for olfaction to their relevant endpoints in the human brain.

Peripheral

The peripheral olfactory system consists mainly of the nostrils, ethmoid bone, nasal cavity, and the olfactory epithelium (layers of thin tissue covered in mucus that line the nasal cavity). The primary components of the layers of epithelial tissue are the mucous membranes, olfactory glands, olfactory neurons, and nerve fibers of the olfactory nerves. [1]

Odor molecules can enter the peripheral pathway and reach the nasal cavity either through the nostrils when inhaling (olfaction) or through the throat when the tongue pushes air to the back of the nasal cavity while chewing or swallowing (retro-nasal olfaction). [2] Inside the nasal cavity, mucus lining the walls of the cavity dissolves odor molecules. Mucus also covers the olfactory epithelium, which contains mucous membranes that produce and store mucus, and olfactory glands that secrete metabolic enzymes found in the mucus. [3]

Transduction

Action potential propagated by olfactory stimuli in an axon. Action potential propagation animation.gif
Action potential propagated by olfactory stimuli in an axon.

Olfactory sensory neurons in the epithelium detect odor molecules dissolved in the mucus and transmit information about the odor to the brain in a process called sensory transduction. [4] [5] Olfactory neurons have cilia (tiny hairs) containing olfactory receptors that bind to odor molecules, causing an electrical response that spreads through the sensory neuron to the olfactory nerve fibers at the back of the nasal cavity. [2]

Olfactory nerves and fibers transmit information about odors from the peripheral olfactory system to the central olfactory system of the brain, which is separated from the epithelium by the cribriform plate of the ethmoid bone. Olfactory nerve fibers, which originate in the epithelium, pass through the cribriform plate, connecting the epithelium to the brain's limbic system at the olfactory bulbs. [6]

Central

Details of olfaction system 1403 Olfaction.jpg
Details of olfaction system

The main olfactory bulb transmits pulses to both mitral and tufted cells, which help determine odor concentration based on the time certain neuron clusters fire (called 'timing code'). These cells also note differences between highly similar odors and use that data to aid in later recognition. The cells are different with mitral having low firing-rates and being easily inhibited by neighboring cells, while tufted have high rates of firing and are more difficult to inhibit. [7] [8] [9] [10] How the bulbar neural circuit transforms odor inputs to the bulb to the bulbar responses that are sent to the olfactory cortex can be partly understood by a mathematical model. [11]

The uncus houses the olfactory cortex which includes the piriform cortex (posterior orbitofrontal cortex), amygdala, olfactory tubercle, and parahippocampal gyrus.

The olfactory tubercle connects to numerous areas of the amygdala, thalamus, hypothalamus, hippocampus, brain stem, retina, auditory cortex, and olfactory system. In total it has 27 inputs and 20 outputs. An oversimplification of its role is to state that it: checks to ensure odor signals arose from actual odors rather than villi irritation, regulates motor behavior (primarily social and stereotypical) brought on by odors, integrates auditory and olfactory sensory info to complete the aforementioned tasks, and plays a role in transmitting positive signals to reward sensors (and is thus involved in addiction). [12] [13] [14]

The amygdala (in olfaction) processes pheromone, allomone, and kairomone (same-species, cross-species, and cross-species where the emitter is harmed and the sensor is benefited, respectively) signals. Due to cerebrum evolution this processing is secondary and therefore is largely unnoticed in human interactions. [15] Allomones include flower scents, natural herbicides, and natural toxic plant chemicals. The info for these processes comes from the vomeronasal organ indirectly via the olfactory bulb. [16] The main olfactory bulb's pulses in the amygdala are used to pair odors to names and recognize odor to odor differences. [17] [18]

Stria terminalis, specifically bed nuclei (BNST), act as the information pathway between the amygdala and hypothalamus, as well as the hypothalamus and pituitary gland. BNST abnormalities often lead to sexual confusion and immaturity. BNST also connects to the septal area, rewarding sexual behavior. [19] [20]

Mitral pulses to the hypothalamus promote/discourage feeding, whereas accessory olfactory bulb pulses regulate reproductive and odor-related-reflex processes.

The hippocampus (although minimally connected to the main olfactory bulb) receives almost all of its olfactory information via the amygdala (either directly or via the BNST). The hippocampus forms new and reinforces existing memories.

Similarly, the parahippocampus encodes, recognizes and contextualizes scenes. [21] The parahippocampal gyrus houses the topographical map for olfaction.

The orbitofrontal cortex (OFC) is heavily correlated with the cingulate gyrus and septal area to act out positive/negative reinforcement. The OFC is the expectation of reward/punishment in response to stimuli. The OFC represents the emotion and reward in decision making. [22]

The anterior olfactory nucleus distributes reciprocal signals between the olfactory bulb and piriform cortex. [23] The anterior olfactory nucleus is the memory hub for smell. [24]

When different odor objects or components are mixed, humans and other mammals sniffing the mixture (presented by, e.g., a sniff bottle) are often unable to identify the components in the mixture even though they can recognize each individual component presented alone. [25] This is largely because each odor sensory neuron can be excited by multiple odor components. It has been proposed that, in an olfactory environment typically composed of multiple odor components (e.g., odor of a dog entering a kitchen that contains a background coffee odor), feedback from the olfactory cortex to the olfactory bulb [26] suppresses the pre-existing odor background (e.g., coffee) via olfactory adaptation, [27] so that the newly arrived foreground odor (e.g., dog) can be singled out from the mixture for recognition. [28]

1: Olfactory bulb 2: Mitral cells 3: Bone 4: Nasal epithelium 5: Glomerulus 6: Olfactory receptor cells Olfactory system.svg
1: Olfactory bulb 2: Mitral cells 3: Bone 4: Nasal epithelium 5: Glomerulus 6: Olfactory receptor cells

Clinical significance

Loss of smell is known as anosmia. Anosmia can occur on both sides or a single side.

Olfactory problems can be divided into different types based on their malfunction. The olfactory dysfunction can be total (anosmia), incomplete (partial anosmia, hyposmia, or microsmia), distorted (dysosmia), or can be characterized by spontaneous sensations like phantosmia. An inability to recognize odors despite a normally functioning olfactory system is termed olfactory agnosia. Hyperosmia is a rare condition typified by an abnormally heightened sense of smell. Like vision and hearing, the olfactory problems can be bilateral or unilateral meaning if a person has anosmia on the right side of the nose but not the left, it is a unilateral right anosmia. On the other hand, if it is on both sides of the nose it is called bilateral anosmia or total anosmia. [29]

Destruction to olfactory bulb, tract, and primary cortex (brodmann area 34) results in anosmia on the same side as the destruction. Also, irritative lesion of the uncus results in olfactory hallucinations.

Damage to the olfactory system can occur by traumatic brain injury, cancer, infection, inhalation of toxic fumes, or neurodegenerative diseases such as Parkinson's disease and Alzheimer's disease. These conditions can cause anosmia. In contrast, recent finding suggested the molecular aspects of olfactory dysfunction can be recognized as a hallmark of amyloidogenesis-related diseases and there may even be a causal link through the disruption of multivalent metal ion transport and storage. [30] Doctors can detect damage to the olfactory system by presenting the patient with odors via a scratch and sniff card or by having the patient close their eyes and try to identify commonly available odors like coffee or peppermint candy. Doctors must exclude other diseases that inhibit or eliminate 'the sense of smell' such as chronic colds or sinusitus before making the diagnosis that there is permanent damage to the olfactory system.

Prevalence of olfactory dysfunction in the general US population was assessed by questionnaire and examination in a national health survey in 2012–2014. [31] Among over a thousand persons aged 40 years and older, 12.0% reported a problem with smell in the past 12 months and 12.4% had olfactory dysfunction on examination. Prevalence rose from 4.2% at age 40–49 to 39.4% at 80 years and older and was higher in men than women, in blacks and Mexican Americans than in whites and in less than more educated. Of concern for safety, 20% of persons aged 70 and older were unable to identify smoke and 31%, natural gas.

Causes of olfactory dysfunction

Vesalius' Fabrica, 1543. Human Olfactory bulbs and Olfactory tracts outlined in red 1543,Vesalius'OlfactoryBulbs.jpg
Vesalius' Fabrica, 1543. Human Olfactory bulbs and Olfactory tracts outlined in red

The common causes of olfactory dysfunction: advanced age, viral infections, exposure to toxic chemicals, head trauma, and neurodegenerative diseases. [29]

Age

Age is the strongest reason for olfactory decline in healthy adults, having even greater impact than does cigarette smoking. Age-related changes in smell function often go unnoticed and smell ability is rarely tested clinically unlike hearing and vision. 2% of people under 65 years of age have chronic smelling problems. This increases greatly between people of ages 65 and 80 with about half experiencing significant problems smelling. Then for adults over 80, the numbers rise to almost 75%. [32] The basis for age-related changes in smell function include closure of the cribriform plate, [29] and cumulative damage to the olfactory receptors from repeated viral and other insults throughout life.

Viral infections

The most common cause of permanent hyposmia and anosmia are upper respiratory infections. Such dysfunctions show no change over time and can sometimes reflect damage not only to the olfactory epithelium, but also to the central olfactory structures as a result of viral invasions into the brain. Among these virus-related disorders are the common cold, hepatitis, influenza and influenza-like illness, as well as herpes. Notably, COVID-19 is associated with olfactory disturbance. [33] Most viral infections are unrecognizable because they are so mild or entirely asymptomatic. [29]

Exposure to toxic chemicals

Chronic exposure to some airborne toxins such as herbicides, pesticides, solvents, and heavy metals (cadmium, chromium, nickel, and manganese), can alter the ability to smell. [34] These agents not only damage the olfactory epithelium, but they are likely to enter the brain via the olfactory mucosa. [35]

Head trauma

Trauma-related olfactory dysfunction depends on the severity of the trauma and whether strong acceleration/deceleration of the head occurred. Occipital and side impact causes more damage to the olfactory system than frontal impact. [36] However, recent evidence from individuals with traumatic brain injury suggests that smell loss can occur with changes in brain function outside of olfactory cortex. [37]

Neurodegenerative diseases

Neurologists have observed that olfactory dysfunction is a cardinal feature of several neurodegenerative diseases such as Alzheimer's disease and Parkinson's disease. Most of these patients are unaware of an olfactory deficit until after testing where 85% to 90% of early-stage patients showed decreased activity in central odor processing structures. [38]

Other neurodegenerative diseases that affect olfactory dysfunction include Huntington's disease, multi-infarct dementia, amyotrophic lateral sclerosis, and schizophrenia. These diseases have more moderate effects on the olfactory system than Alzheimer's or Parkinson's diseases. [39] Furthermore, progressive supranuclear palsy and parkinsonism are associated with only minor olfactory problems. These findings have led to the suggestion that olfactory testing may help in the diagnosis of several different neurodegenerative diseases. [40]

Neurodegenerative diseases with well-established genetic determinants are also associated with olfactory dysfunction. Such dysfunction, for example, is found in patients with familial Parkinson's disease and those with Down syndrome. [41] Further studies have concluded that the olfactory loss may be associated with intellectual disability, rather than any Alzheimer's disease-like pathology. [42]

Huntington's disease is also associated with problems in odor identification, detection, discrimination, and memory. The problem is prevalent once the phenotypic elements of the disorder appear, although it is unknown how far in advance the olfactory loss precedes the phenotypic expression. [29]

History

Linda B. Buck and Richard Axel won the 2004 Nobel Prize in Physiology or Medicine for their work on the olfactory system.

See also

Related Research Articles

<span class="mw-page-title-main">Anosmia</span> Inability to smell

Anosmia, also known as smell blindness, is the loss of the ability to detect one or more smells. Anosmia may be temporary or permanent. It differs from hyposmia, which is a decreased sensitivity to some or all smells.

<span class="mw-page-title-main">Olfactory nerve</span> Cranial nerve I, for smelling

The olfactory nerve, also known as the first cranial nerve, cranial nerve I, or simply CN I, is a cranial nerve that contains sensory nerve fibers relating to the sense of smell.

<span class="mw-page-title-main">Vomeronasal organ</span> Smell sense organ above the roof of the mouth

The vomeronasal organ (VNO), or Jacobson's organ, is the paired auxiliary olfactory (smell) sense organ located in the soft tissue of the nasal septum, in the nasal cavity just above the roof of the mouth in various tetrapods. The name is derived from the fact that it lies adjacent to the unpaired vomer bone in the nasal septum. It is present and functional in all snakes and lizards, and in many mammals, including cats, dogs, cattle, pigs, and some primates. Some humans may have physical remnants of a VNO, but it is vestigial and non-functional.

<span class="mw-page-title-main">Olfactory bulb</span> Neural structure

The olfactory bulb is a neural structure of the vertebrate forebrain involved in olfaction, the sense of smell. It sends olfactory information to be further processed in the amygdala, the orbitofrontal cortex (OFC) and the hippocampus where it plays a role in emotion, memory and learning.

<span class="mw-page-title-main">Olfactory epithelium</span> Specialised epithelial tissue in the nasal cavity that detects odours

The olfactory epithelium is a specialized epithelial tissue inside the nasal cavity that is involved in smell. In humans, it measures 5 cm2 (0.78 sq in) and lies on the roof of the nasal cavity about 7 cm (2.8 in) above and behind the nostrils. The olfactory epithelium is the part of the olfactory system directly responsible for detecting odors.

<span class="mw-page-title-main">Glomerulus (olfaction)</span>

The glomerulus is a spherical structure located in the olfactory bulb of the brain where synapses form between the terminals of the olfactory nerve and the dendrites of mitral, periglomerular and tufted cells. Each glomerulus is surrounded by a heterogeneous population of juxtaglomerular neurons and glial cells.

Parosmia is a dysfunctional smell detection characterized by the inability of the brain to correctly identify an odor's "natural" smell. Instead, the natural odor is usually transformed into an unpleasant aroma, typically a "burned", "rotting", "fecal", or "chemical" smell. There can also be rare instances of a pleasant odor called euosmia. The condition was rare and little-researched until it became relatively more widespread since 2020 as a side effect of COVID-19.

In medicine and anatomy, the special senses are the senses that have specialized organs devoted to them:

<span class="mw-page-title-main">Olfactory tubercle</span> Area at the bottom of the forebrain

The olfactory tubercle (OT), also known as the tuberculum olfactorium, is a multi-sensory processing center that is contained within the olfactory cortex and ventral striatum and plays a role in reward cognition. The OT has also been shown to play a role in locomotor and attentional behaviors, particularly in relation to social and sensory responsiveness, and it may be necessary for behavioral flexibility. The OT is interconnected with numerous brain regions, especially the sensory, arousal, and reward centers, thus making it a potentially critical interface between processing of sensory information and the subsequent behavioral responses.

Phantosmia, also called an olfactory hallucination or a phantom odor, is smelling an odor that is not actually there. This is intrinsically suspicious as the formal evaluation and detection of relatively low levels of odour particles is itself a very tricky task in air epistemology. It can occur in one nostril or both. Unpleasant phantosmia, cacosmia, is more common and is often described as smelling something that is burned, foul, spoiled, or rotten. Experiencing occasional phantom smells is normal and usually goes away on its own in time. When hallucinations of this type do not seem to go away or when they keep coming back, it can be very upsetting and can disrupt an individual's quality of life.

The primary olfactory cortex (POC) is a portion of the cerebral cortex. It is found in the inferior part of the temporal lobe of the brain. It receives input from the olfactory tract. It is involved in the sense of smell (olfaction).

Hyposmia, or microsmia, is a reduced ability to smell and to detect odors. A related condition is anosmia, in which no odors can be detected. Some of the causes of olfaction problems are allergies, nasal polyps, viral infections and head trauma. In 2012 an estimated 9.8 million people aged 40 and older in the United States had hyposmia and an additional 3.4 million had anosmia/severe hyposmia.

Olfactory fatigue, also known as odor fatigue, olfactory adaptation, and noseblindness, is the temporary, normal inability to distinguish a particular odor after a prolonged exposure to that airborne compound. For example, when entering a restaurant initially the odor of food is often perceived as being very strong, but after time the awareness of the odor normally fades to the point where the smell is not perceptible or is much weaker. After leaving the area of high odor, the sensitivity is restored with time. Anosmia is the permanent loss of the sense of smell, and is different from olfactory fatigue.

Dysosmia is a disorder described as any qualitative alteration or distortion of the perception of smell. Qualitative alterations differ from quantitative alterations, which include anosmia and hyposmia. Dysosmia can be classified as either parosmia or phantosmia. Parosmia is a distortion in the perception of an odorant. Odorants smell different from what one remembers. Phantosmia is the perception of an odor when no odorant is present. The cause of dysosmia still remains a theory. It is typically considered a neurological disorder and clinical associations with the disorder have been made. Most cases are described as idiopathic and the main antecedents related to parosmia are URTIs, head trauma, and nasal and paranasal sinus disease. Dysosmia tends to go away on its own but there are options for treatment for patients that want immediate relief.

<span class="mw-page-title-main">Sense of smell</span> Sense that detects smells

The sense of smell, or olfaction, is the special sense through which smells are perceived. The sense of smell has many functions, including detecting desirable foods, hazards, and pheromones, and plays a role in taste.

Olfactory memory refers to the recollection of odors. Studies have found various characteristics of common memories of odor memory including persistence and high resistance to interference. Explicit memory is typically the form focused on in the studies of olfactory memory, though implicit forms of memory certainly supply distinct contributions to the understanding of odors and memories of them. Research has demonstrated that the changes to the olfactory bulb and main olfactory system following birth are extremely important and influential for maternal behavior. Mammalian olfactory cues play an important role in the coordination of the mother infant bond, and the following normal development of the offspring. Maternal breast odors are individually distinctive, and provide a basis for recognition of the mother by her offspring.

<span class="mw-page-title-main">Sniffing (behavior)</span> Nasal inhalation to sample odors

Sniffing is a perceptually-relevant behavior, defined as the active sampling of odors through the nasal cavity for the purpose of information acquisition. This behavior, displayed by all terrestrial vertebrates, is typically identified based upon changes in respiratory frequency and/or amplitude, and is often studied in the context of odor guided behaviors and olfactory perceptual tasks. Sniffing is quantified by measuring intra-nasal pressure or flow or air or, while less accurate, through a strain gauge on the chest to measure total respiratory volume. Strategies for sniffing behavior vary depending upon the animal, with small animals displaying sniffing frequencies ranging from 4 to 12 Hz but larger animals (humans) sniffing at much lower frequencies, usually less than 2 Hz. Subserving sniffing behaviors, evidence for an "olfactomotor" circuit in the brain exists, wherein perception or expectation of an odor can trigger brain respiratory center to allow for the modulation of sniffing frequency and amplitude and thus acquisition of odor information. Sniffing is analogous to other stimulus sampling behaviors, including visual saccades, active touch, and whisker movements in small animals. Atypical sniffing has been reported in cases of neurological disorders, especially those disorders characterized by impaired motor function and olfactory perception.

The University of Pennsylvania Smell Identification Test (UPSIT) is a test that is commercially available for smell identification to test the function of an individual's olfactory system.

Retronasal smell, retronasal olfaction, is the ability to perceive flavor dimensions of foods and drinks. Retronasal smell is a sensory modality that produces flavor. It is best described as a combination of traditional smell and taste modalities. Retronasal smell creates flavor from smell molecules in foods or drinks shunting up through the nasal passages as one is chewing. When people use the term "smell", they are usually referring to "orthonasal smell", or the perception of smell molecules that enter directly through the nose and up the nasal passages. Retronasal smell is critical for experiencing the flavor of foods and drinks. Flavor should be contrasted with taste, which refers to five specific dimensions: (1) sweet, (2) salty, (3) bitter, (4) sour, and (5) umami. Perceiving anything beyond these five dimensions, such as distinguishing the flavor of an apple from a pear for example, requires the sense of retronasal smell.

Smell training or olfactory training is the act of regularly sniffing or exposing oneself to robust aromas with the intention of regaining a sense of smell. The stimulating smells used are often selected from major smell categories, such as aromatic, flowery, fruity, and resinous. Using strong scents, the patient is asked to sniff each different smell for a minimum of 20 seconds, no less than two times per day, for three to six months or more. It is used as a rehabilitative therapy to help people who have anosmia or post-viral olfactory dysfunction, a symptom of COVID-19. It was considered a promising experimental treatment in a 2017 meta-analysis.

References

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  31. ↑ Hoffman, Howard; Rawal, Shristi; Li, Chuan-Ming; Duffy, Valerie (June 2016). "New chemosensory component in the U.S. National Health and Nutrition Examination Survey (NHANES): first-year results for measured olfactory dysfunction". Rev Endocr Metab Disord. 17 (2): 221–240. doi:10.1007/s11154-016-9364-1. PMC   5033684 . PMID   27287364.
  32. ↑ Doty, Richard L.; Shaman, Paul; Dann, Michael (March 1984). "Development of the university of pennsylvania smell identification test: A standardized microencapsulated test of olfactory function". Physiology & Behavior. 32 (3): 489–502. doi:10.1016/0031-9384(84)90269-5. PMID   6463130. S2CID   30923277.
  33. ↑ Parma V (June 2020). "More than smell–COVID-19 is associated with severe impairment of smell, taste, and chemesthesis". Chemical Senses. bjaa041 (7): 609–622. doi: 10.1093/chemse/bjaa041 . PMC   7337664 . PMID   32564071.
  34. ↑ Doty, RL; Hastings, L. (2001). "Neurotoxic exposure and olfactory impairment". Clin Occupat Environ Med. 1: 547–575.
  35. ↑ Tjalve, H.; Henriksson, J.; Tallkvist, J.; Larsson, B. S.; Lindquist, N. G. (1996). "Uptake of manganese and cadmium from the nasal mucosa into the central nervous system via olfactory pathways in rats". Pharmacology & Toxicology. 79 (6): 347–356. doi:10.1111/j.1600-0773.1996.tb00021.x. PMID   9000264.
  36. ↑ Doty, R. L.; Yousem, D. M.; Pham, L. T.; Kreshak, A. A.; Geckle, R.; Lee, W. W. (1997). "Olfactory dysfunction in patients with head trauma". Arch Neurol. 54 (9): 1131–1140. doi:10.1001/archneur.1997.00550210061014. PMID   9311357.
  37. ↑ Pellegrino, Robert (17 February 2021). "Post-traumatic olfactory loss and brain response beyond olfactory cortex". Scientific Reports. 11 (1): 4043. Bibcode:2021NatSR..11.4043P. doi: 10.1038/s41598-021-83621-2 . PMC   7889874 . PMID   33597627.
  38. ↑ Quinn, N P; Rossor, M N; Marsden, C D (1 January 1987). "Olfactory threshold in Parkinson's disease". Journal of Neurology, Neurosurgery & Psychiatry. 50 (1): 88–89. doi:10.1136/jnnp.50.1.88. PMC   1033256 . PMID   3819760.
  39. ↑ Doty, Richard L.; Bromley, Steven M.; Stern, Matthew B. (March 1995). "Olfactory Testing as an Aid in the Diagnosis of Parkinson's Disease: Development of Optimal Discrimination Criteria". Neurodegeneration. 4 (1): 93–97. doi: 10.1006/neur.1995.0011 . PMID   7600189.
  40. ↑ Doty, R. L.; Golbe, L. I.; McKeown, D. A.; Stern, M. B.; Lehrach, C. M.; Crawford, D. (1 May 1993). "Olfactory testing differentiates between progressive supranuclear palsy and idiopathic Parkinson's disease". Neurology. 43 (5): 962–965. doi:10.1212/WNL.43.5.962. PMID   8492953. S2CID   41865918.
  41. ↑ CHEN, M; LANDER, T; MURPHY, C (May 2006). "Nasal health in Down syndrome: A cross-sectional study". Otolaryngology–Head and Neck Surgery. 134 (5): 741–745. doi:10.1016/j.otohns.2005.12.035. PMID   16647527. S2CID   21198608.
  42. ↑ McKeown, D A; Doty, R L; Perl, D P; Frye, R E; Simms, I; Mester, A (1 October 1996). "Olfactory function in young adolescents with Down's syndrome". Journal of Neurology, Neurosurgery & Psychiatry. 61 (4): 412–414. doi:10.1136/jnnp.61.4.412. PMC   486586 . PMID   8890783.
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