Table 5.

Results of PRISMA Showing the Impact of Perinatal Marijuana and Perinatal Alcohol in the Hippocampal Formation of Adult Rats and Mice. A/M Indicates if the Perinatal Exposure is Alcohol(A) or Marijuana(M). M and F in the “Main Finding” Column Indicate When There are Sex Differences in the Results. Exposure and Test Ages are Reported as Embryonic (E) Days of Age or Postnatal (P) Days of Age.

	A/M	Exposure Age	Model	Sex	Test Age	What was Investigated?	Marker/ Stain Used	Hippocampal Subregion	Main Finding
1	A	P2-P9	Mouse	MF	P90	GABA Interneurons	Venus-VGAT	CA1	Decreased in M
								CA3	Decreased in M
								GCL	Decreased in MF
								Hilus	Decreased in M
2	A	E7-E21	Rat	M	P60	Type 2b INP to Immature Granule Neuron	DCX	CA1 CA2 + 3	No Change No Change
								DG	No Change
3	M	E10.5–E17.5	Mouse	MF	P20-P60	Cannabinoid receptor type 1	CB1R	CA1	Decrease in M
						Cholecystokinin interneurons	CCK	CA1	Decrease in M
4	A	E1–21	Rat	M	P78–82	Dividing Cells	BrdU	DG	No Change
						Type 2b INP to IGN	DCX	DG	No Change
						Dividing Cells	Ki-67	DG	No Change
					P115	Dividing Cells	BrdU, P80	DG	Decrease
						Type 2b INP to IGN	DCX	DG	No Change
5	A	E1-P9	Rat	MF	P386	Type 2b INP to IGN	DCX	DG	Decrease in F
						Dividing Cells	Ki-67	DG	No Change
6	A	P4–9	Rat	MF	P60	Dividing Cells	BrdU 2 hours	DG	No Change
						Dividing Cells	Ki-67	DG	No Change
						Type 2b INP to Mature Granule Neuron	NeuroD	DG	Decrease
					P90	Dividing Cells	BrdU P60	DG	No Change
						Dividing Cells	Ki-67	DG	No Change
						Type 2b INP to Mature Granule Neuron	NeuroD	DG	Decrease
7	A	P4–9	Rat	M	P80	Dividing Cells	BrdU	DG	Decrease
					P50	Dividing Cells	BrdU	DG	No Change
					P50	Dividing Cells	Ki-67	DG	No Change
8	A	E9–20	Rat	M	P84	GABAergic Mature Neurons	NeuN and GAD67	CA3	Increase
								DG	Increase
						Glutamatergic Mature Neuron	NeuN and Glutamate	CA3 DG	Decrease Decrease
9	A	E7-E17	Mouse	MF	P56	Type 2b INP to Immature Granule Neuron	DCX	DG	Decrease
						Dividing Cells	Ki-67	DG	No Change
10	A	E1–21	Rat	M	P60–65	Dividing Cells	BrdU	GCL	No Change
								Hilus	No Change
					P81–86		BrdU P60–65	GCL	No Change
								Hilus	No Change
11	M	E5.5–E17.5	Rat	M	P120	CB1-positive Boutons	CB1R	CA1	Increase
12	A	E1–21	Rat	F	P60–65	Dividing Cells	BrdU	GCL	No Change
					P81–86	Dividing Cells	BrdU P60–65	GCL	No Change
						0- to 3-week-old Glia	GFAP/BrdU P60–65	GCL	No Change
						0- to 3-week-old Mature Granule Neurons	NeuN/BrdU P60–65	GCL	No Change
13	M	E10.5–E18.5	Mouse	MF	P30	Caudal Ganglionic Eminence–derived Interneurons	GFP (5HT3AR-GFP transgenic line)	DG/Hilar Border	Decrease
						Medial Ganglionic Eminence–derived Interneurons	GFP (NKX2.1-cre: RCE-GFP transgenic line)	DG/Hilar Border	No Change

CA1, cornu ammonis area 1; CA2, cornu ammonis area 2; CA3, cornu ammonis area 3; DG, dentate gyrus; GABA, gamma-aminobutyric acid; GCL, granule cell layer; IGN, Immature granule neurons; INP, Immature Neural Progenitor.

Marker purposes are as follows: BrdU, bromodeoxyuridine, a thymidine analogue that labels DNA synthesis; CB1R, cannabinoid receptor type 1; DCX, doublecortin, a neuronal migration protein; GAD67, glutamate decarboxylase 67 kilodalton isoform; GFP, green fluorescent protein; Ki-67, antigen Ki-67, a marker of proliferation; NeuN, neuronal nuclei, a mature neuron marker; NeuroD, neurogenic differentiation factor 2, a marker of type 2b immature up to mature granule neurons; Venus-VGAT, a transgenic construct that labels GABAergic neurons.

^1.Bird et al. (2018); 2. Elibol-Can et al. (2014); 3. de Salas-Quiroga et al. (2020); 4. Gil-Mohapel et al. (2011); 5. Gil-Mohapel et al. (2014); 6. Hamilton et al. (2011); 7. Klintsova et al. (2007); 8. Lu et al. (2018); 9. Olateju et al. (2018); 10. Sliwowska et al. (2010); 11. Tortoriello et al. (2014); 12. Uban et al. (2010); 13. Vargish et al. (2017).