Table 1.

Summary of the major groups of animals described in this review, and their indenting/invaginating presynaptic terminals

Group	Motor terminal synapses	Sensory cell synapses	CNS synapses
Porifera (sponges)	Unknown, but with invaginating processes1	Unknown, but with invaginating processes	Unknown, but with invaginating processes
Ctenophora (comb jellies)	NMJs indented2	–	Some deeply indented3
Cnidaria (jellyfish, sea anemones, corals, hydroids)	NMJs occasionally indented; also axon wrapped in muscle processes4	Nematocyte (stinging hair cell) with basal indented efferent5 or basal tunnel with afferents + efferents6	–
Flatworms (Platyhelminthes)	NMJs indented or invaginated; associated with muscle processes7	–	Some invaginated8
Nematodes (roundworms) and Gastrotricha (hairybacks)	Unknown; synapses at the ends of muscle processes9	–	–
Chaetognatha (arrow worms) and rotifers	Some deeply indented/partly invaginated NMJs10; arrow worms with distinctive subsynaptic apparatus11	–	–
Phoronida (horseshoe worms)	Unknown12	–	–
Entoprocta and Annelida (leeches, earthworms)	Some indented or deeply indented NMJs13	–	–
Mollusca (octopi, squid, snails, mussels, chitons)	NMJs often indented or invaginated14; invaginated terminals in salivary glands (ex) of snails and octopi15, and in dorsal body gland (en) of snails16	Tunnel fibers and finger twigs invaginate into photoreceptor presynaptic bags/carrots (octopi and squid)17	Presynaptic processes from afferent giant axons invaginate into efferent giant axons (squid)18
Arthropoda—Chelicerata (spiders, scorpions, mites)	NMJs often indented in spiders and scorpions19; invaginated in a tick20; horseshoe crab with invaginated terminal in muscle evagination21; invaginated terminal in salivary/silk gland (ex) of mite22	In jumping spiders, retinal terminals invaginated by processes from presynaptic second-order terminals23; also, wolf spiders have invaginating postsynaptic complex in retinal terminals with possible efferent components24	–
Arthropoda—Crustacea (crayfish, lobsters, crabs)	Many deeply invaginated NMJs with elaborate SSR25; double invaginated terminals in labral glands (ex) of water flea26	Crayfish and lobster have invaginating postsynaptic complex in retinal terminals with possible efferent components27	Crayfish have indentions/invaginations between giant axons, with combinations of electrical and chemical transmission28
Arthropoda—Insecta (Drosophila, moths, beetles, cicadas, etc.)	Many deeply invaginated NMJs with elaborate SSR29; Indented terminals in prothoracic gland (en) of wax moth30	–	Invaginating finger projections from giant fibers into interneurons may be presynaptic in Drosophila31
Echinodermata (starfish, sea urchins, sea cucumbers)	Axons may be invaginated in muscle of sea cucumber32; terminals can be invaginated in sea urchin muscle fibers33	–	–
Invertebrate chordates (sea squirts or ascidians, amphioxus or lancelets)	Unknown; in lancelets, synapses at the ends of muscle processes34	Ascidian coronal organ hair cells with basal groove with afferent + efferent terminals35	Larval lancelets with juxta-reticular junctions that may invaginate into cell bodies36
Vertebrata—Agnatha (hagfish, lampreys)	Deeply invaginated NMJs with Schwann cell plug in hagfish37; deeply indented in lampreys38	Invaginating synaptic complex in photoreceptor cells may have some efferents39	Vestibular nerve spoon endings invaginate into vestibular neuron somas in lamprey larvae40
Vertebrata—sharks and bony fish	Some deeply invaginated NMJs with extensive SJFs in sharks41; indented in bony fish-only a few with prominent SJFs42; some deeply invaginated cardiac NMJs in trout43	Electroreceptors with presynaptic ribbon/sheet/rod44; in retina, invaginated horizontal cell processes provide negative feedback to photoreceptor cells45	–
Vertebrata—Amphibians (frogs, toads, salamanders, newts)	Some indented NMJs with Schwann fingers and prominent SJFs46; moderately deep indentions of smooth muscle of frog/toad intestines47; indented terminals in pancreatic Islets (en) of toad48, and neuroepithelial body (en) in lung of salamander49	In salamanders, vesicle-filled invaginating processes in photoreceptor cells may be efferents50; horizontal cell processes provide negative feedback to photoreceptor cells51	–
Vertebrata—reptiles and birds	Indented and occasionally invaginated NMJs in some reptiles52; only shallow indentions in birds53; indented terminals in acinar cells (ex) in pancreas of chicken54	Indenting efferents in auditory hair cells of pigeon55; in turtles, horizontal cell processes provide negative feedback to photoreceptor cells56	In birds, reciprocal interdigitations in developing auditory nerve endbulbs on neuron somas57
Vertebrata—mammals	NMJs indented and some with invaginations and/or with extensive SJFs58; also for some NMJs in extraocular59, cardiac60 and smooth muscle61; indented or invaginated terminals in various ex/en glands62	Invaginating horizontal cell processes provide negative feedback to photoreceptor cells (including structural studies)63	reciprocal interdigitations in developing auditory nerve endbulbs on neuron somas64; vestibular nerve terminal invaginations into rat lateral vestibular nucleus neuron65; cupshaped spines66; crested dendrites67

Indented ≈ presynaptic processes run in a deep pit or groove; invaginated ≈ presynaptic varicosity is embedded within the postsynaptic process. CNS, central nervous system; en, endocrine gland cells; ex, exocrine gland cells; NMJs, neuromuscular junctions; SSR, subsynaptic reticulum; SJFs, subjunctional folds; dash indicates no information found

¹Pavans de Ceccatty (1966)

²Horridge (1965)

³Hernandez-Nicaise (1973)

⁴Spencer (1979)

⁵Westfall et al. (1971)

⁶Holtmann and Thurm (2001a, b)

⁷Pan (1980)

⁸Petralia et al. (2015)

⁹Reger (1965)

¹⁰Clément (1977)

¹¹Duvert and Barets (1983)

¹²Lacalli (1990)

¹³Reger (1969), Rosenbluth (1973), Yaksta-Sauerland and Coggeshall (1973)

¹⁴Graziadei (1966), Barber and Graziadei (1967), Rogers (1969), Økland (1980), Elekes and Ude (1994)

¹⁵Ducros (1972), Elekes and Ude (1994)

¹⁶Moraes et al. (2010)

¹⁷Dilly et al. (1963), Case et al. (1972), Cohen (1973), Haghighat et al. (1984)

¹⁸Castejón and Villegas (1964)

¹⁹Melamed and Trujillo-Cenoz (1971), Smith (1971), Fourtner and Sherman (1973), Sherman (1973)

²⁰Hart et al. (1980)

²¹Lang (1972), Sherman and Fourtner (1972), Fourtner and Sherman (1973)

²²Filimonova and Amosova (2015)

²³Oberdorfer (1977)

²⁴Trujillo-Cenoz and Melamed (1967)

²⁵Hoyle and McNeill (1968), Jahromi and Atwood (1974), Govind et al. (1995)

²⁶Zeni and Zaffagnini (1988)

²⁷Hamori and Horridge (1966), Hafner (1974)

²⁸Hama (1961), Heitler et al. (1985)

²⁹Edwards et al. (1958b), Smith (1960), Rheuben and Reese (1978), Rheuben (1985), Prokop (1999), Wagner et al. (2015)

³⁰Benedeczky et al. (1980)

³¹Blagburn et al. (1999)

³²Doyle (1967)

³³Cobb and Laverack (1966)

³⁴Flood (1966)

³⁵Burighel et al. (2003), Manni et al. (2006)

³⁶Lacalli (2002)

³⁷Korneliussen (1973a, b)

³⁸Teräväinen (1971)

³⁹Holmberg (1971)

⁴⁰Stefanelli and Caravita (1970)

⁴¹Bone (1972)

⁴²Best and Bone (1973)

⁴³Yamauchi and Burnstock (1968)

⁴⁴Szamier and Wachtel (1969), Szamier and Bennett (1973), Teeter et al. (1980)

⁴⁵Murakami et al. (1982)

⁴⁶Birks et al. (1960); Matthews-Bellinger and Salpeter (1978), Heuser and Reese (1973)

⁴⁷Rogers and Burnstock (1966), Thaemert (1966)

⁴⁸Kobayashi (1966)

⁴⁹Goniakowska-Witalinska et al. (1992)

⁵⁰Dowling and Werblin (1969), Lasansky (1973)

⁵¹Babai and Thoreson (2009)

⁵²Robertson (1956), Hess (1965), Walrond and Reese (1985)

⁵³Hess (1967), Kwong and Gauthier (1987)

⁵⁴Dahl (1973)

⁵⁵Takasaka and Smith (1971)

⁵⁶Tatsukawa et al. (2005)

⁵⁷Jhaveri and Morest (1982), Carr and Boudreau (1996)

⁵⁸Ellisman et al. (1976), Boaro et al. (1998)

⁵⁹Teräväinen (1968a, b)

⁶⁰Trautwein and Uchizono (1963), Hirano and Ogawa (1967), Mochet et al. (1975)

⁶¹Lane and Rhodin (1964), Taxi (1964)

⁶²Bargmann et al. (1967), Hand (1970), Kleitman and Holzwarth (1985), Ju and Zhang (1990)

⁶³Raviola and Gilula (1975); Linberg and Fisher (1988), Babai and Thoreson (2009), Gardner et al. (2015), Kramer and Davenport (2015), Hirano et al. (2016)

⁶⁴Ryugo et al. (2006)

⁶⁵Sotelo and Palay (1968, 1970)

⁶⁶Desmond and Levy (1983), Frotscher and Léránth (1986)

⁶⁷Murray et al. (1979)