Sensory organs

   

Types of sensilla
Two major types of sensilla can be distinguished in the fully developed embryo - external sensory organs, located within the epidermis, and chordotonal organs, located internally in the body wall or close to the somatic muscles.

External sensilla contain one or more bipolar neurons, enclosed by three accessory cells. The cell bodies of bipolar neurons lie beneath the epidermis; their dendrite(s) penetrate the epidermis and terminate in conjunction with the cuticle. Accessory cells are modified epidermal cells which form concentric sheaths around the dendrites and build the stimulus receptor structure. The outer accessory cells form the socket (tormogen cell) and the shaft (trichogen cell) of the sensory organ. The inner cell (thecogen cell) secretes a cuticle-like matrix around the tip of the dendrite(s), called the dendritic cap. Most external sensilla are mechanoreceptors; these include hairs (trichoid sensilla) and an ill-defined type called a "papilla sensillum" or "campaniform sensillum. Mechanoreceptors typically possess a single sensory neuron, although one hair and one papilla sensillum of each abdominal segment are innervated by three neurons each. Another type of sensillum which occurs only in the thorax and the telson has been called a basiconical sensillum, characterized by a club shaped process in an epidermal depression. Basiconical sensilla are innervated by three sensory neurons and are probably hygroreceptors.

Chordotonal organs are stretch receptors attached to the basal (inner) surface of the epidermis. In the embryo, chordotonal organs are formed by one, three or five identical units called scolopidia. Each scolopidium, like the external sensillum, has one bipolar neuron and three accessory cells. Unlike those of external sensilla, accessory cells of chordotonal organs are not organized as sheaths around the sensory neurons, but form ligamentous structures by means of which the chordotonal organs insert at the epidermis.

In addition to the sensilla, which comprise bipolar neurons and accessory cells, several different types of isolated sensory neurons, i.e., devoid of accessory cells, are present internally in the embryo. The neurons possess more than one dendrite, and are therefore referred to as multidendritic neurons. Multidendritic neurons occur as clusters of up to five cells attached to the basal surface of the epidermis or internal organs, such as tracheae, peripheral nerves, and muscles. Three types of multidendritic neurons can be distinguished: those with arborizations underneath the epidermis (da neurons), those innervating the tracheal branches (td neurons), and those with two opposing dendrites (bd neurons).

As a rule, neurons and accessory cells of a given sensillum are derivatives of the same sensory organ progenitor cell (SOP). The progenitor cells of external organs innervated by a single neuron undergo two divisions. The progenitors of chordotonal organs and multidendritic neurons delaminate from the epidermal anlage into the interior of the embryo. Proliferation of the SOPs of chordotonal organs and multidendritic neurons begins after they have delaminated and become attached to the basal surface of the ectoderm. Following delamination, the progenitors of multidendritic neurons undergo one to three further divisions to form clusters of up to five neurons. Progenitors of the tri- and pentascolopidial chordotonal organs have a highly complex proliferation pattern which has not been fully reconstructed. The pattern of proliferation of the progenitors of multiply innervated external sensilla is controversial.

Small head sensilla

The dorsal pharyngeal organ (dpo) and a dorsal pharyngeal monoscolopidial chordotonal organ (pch1) are both derived from the labral segment. The dpo is located posterior to the labral sensory complex and is innervated by three neurons of unknown sensory modality. Two sensory structures, the papilla organ (pao) and an associated organ (ao) are spatially related to the terminal organ. The pao is probably of mandibular origin. It comprises a multiply innervated sensillum in the lateral atrial wall. The hypomaxillary organ (hmo) is a multiply innervated sensillum of unknown sensory modality and segmental origin. It is located close to the labial organ, but its axon projects with the maxillary nerve. The hypopharyngeal organ and the latero-hypopharyngeal organ (lho) are likely derived from the intercalary segment. Since these sensilla are among the first ones to differentiate in the head, their movement from a position flanking the stomodeum (position of the intercalary segment) to the floor of the pharynx can be easily followed. The hypopharyngeal organ is innervated by three or four dendrites. Its axons join an anteriorly directed bundle which runs to the labral nerve; the two or three neurons of the latero-hypopharyngeal organ are located at the junction of both branches.The lateropharyngeal organ (lpo) appears at a relatively early stage in the dorsal ridge which is derived by fusion from the dorsal parts of the labium and maxilla. During head involution, the lpo becomes incorporated into the dorsal pouch. The lpo is located at the lumen of the dorsal pouch, and consists of two or three neurons.

Abdominal segments a1-a7
Ventral group: The ventral group consists of six papilla sensilla (vp1, vp2, vp3, vp4, vp4a, vp5), two monoscolopidial chordotonal organs (vch1 and vch2), and several clusters of multidendritic neurons. The ventralmost papilla sensilla vp1 and vp2, are located in the paraneural space at the posterior border of the corresponding segmental nerve. The neurons of vp3, vch1 and vch2, and vdap form a dense cluster located posteriorly in each segment at the level of the ventral oblique musculature. The axons of vp1-3, vch1 and vch2, and vdap, together with the motor axons innervating the ventral oblique muscle fibres, form the branch "c" of the segmental nerve. A side branch of this axon bundle carries sensory axons of the multidendritic neurons vdaA-D and vbp. The cells of vp4, vp4a, and vdaa are located in close proximity to the intersegmental nerve within the anterior half of each segment. Their axons join branch "b" of the segmental nerve which also carries motor axons to several ventral longitudinal and oblique muscle fibres. Finally, there is the group of three sensory neurons of vp5 and the multidendritic vdap neuron, which are the lateralmost representatives of the ventral group of sensilla and which are located at the lateral boundary of the ventral musculature. Their axons join branch "a" of the segmental nerve.Two multidendritic neurons, the intersegmental bidendritic neuron (isbd) and trachea-associated neuron (istd), are located on the segment boundary. Axons of both neurons form a separate nerve, called the transverse nerve which extends ventrally along the segment boundary and enters the ventral nerve cord at a dorsomedial position.
Lateral group:
The most prominent sensillum of the lateral group of abdominal sensilla is lch5, the pentascolopidial chordotonal organ. Its five scolopidia are located posteriorly in the niche formed between the epidermis and the lateral transverse muscle. These scolopidia are strictly aligned and oriented dorsoposteriorly. The ligament cells anchoring lch5 to the epidermis are very long; they insert at close to the posterior segment boundary at the level of the dorsal muscle fibres DO2. During development the lch5 cluster is born in the dorsal ectoderm. In the thoracic segments the lch5 cluster remains at this position whereas the lch5 cluster moves ventrally in the abdominal segments. Sensory neurons of three external sensilla, lh1, lh2 and lp1, and two multidendritic neurons, ltd and lda, flank the pentascolopidial chordotonal organ at its anterior border. The monoscolopidial chordotonal organ lch1 is located more superficially and dorsally than lch5, being oriented dorso-anteriorly. The axons of all lateral sensilla, except for lch1, join the intersegmental nerve; the lch1 axon projects to join branch "a" of the segmental nerve.
Dorsal group:
The dorsal group consists of four external sensilla, a small and a large hair sensillum (dh1 and dh2) and two papillar sensilla (dp1 and dp2), arranged along a vertical line in the middle of each abdominal segment, between the epidermis and the dorsal acute muscles. The small dorsal hair dh1 is innervated by three neurons, the large dh2, as well as dp1 and dp2, are each in contact with only one neuron. Sensory neurons of all four sensilla form a dense cluster with five multidendritic neurons (ddaA-E). A sixth multidendritic, bipolar neuron located ventral to this cluster (dbp) forms conspicuous longitudinal processes which span the entire segment. Axons of all dorsal sensilla course through the intersegmental nerve.
Thoracic segments
Ventral group:
The ventral group consists of five sensilla in each thoracic segment: two papillar sensilla (vp1 and vp2), a monoscolopidial chordotonal organ (vch1), a basiconical sensillum (vbd) and Keilin's organ (ko). The cell bodies of the neurons of vbd and vp2, together with four multidendritic neurons (vdaA-D), are grouped in a somewhat irregularly shaped cluster in the anterior half of the segment, at the level of the ventral oblique muscles (VO1-3). The five neurons associated with Keilin's organ and the monoscolopidial organ vch1 can be found more posteriorly. These neurons form part of the leg imaginal disc and persist into the adult period.
Lateral group:
The patterns of sensilla of the lateral and dorsal group differ in the three thoracic segments. In the prothorax, the lateral group comprises a tight cluster of cells formed by papillar sensilla lp1 and lp2, hair sensillum lh1, a triscolopidial chordotonal organ lch3, and four multidendritic neurons (ldaA-D). Strikingly, the axons of lch3 join the segmental nerve of the mesothoracic segment to course towards the CNS. In addition, there are two more papillar sensilla (px, py) close to the anterior boundary of the prothorax. In the mesothorax and metathorax these two papillae are absent and instead of the lateral triscolopidial chordotonal organ, there is a basiconical sensillum (lbd).
Dorsal group:
In the prothorax, the dorsal group of sensilla comprises hair sensilla dh1 and dh2, with one neuron each; three papillae, dp1-dp3, with one neuron each; a triscolopidial chordotonal organ (dch3), and a dorsal basiconical sensillum (dbd). Clustered around the neurons of these sensilla, there are six multidendritic neurons (ddaA-E; dbp). In mesothorax and metathorax, the dorsal basiconical sensillum is missing.
The innervation of thoracic sensory organs follows the same scheme as that of abdominal sensilla: the ventral group sends its axons through two different branches into the posterior fascicle or the segmental nerve. The axons of the lateral and dorsal group course through the intersegmental nerve.